More stories

  • in

    Transcriptional response to prolonged perchlorate exposure in the methanogen Methanosarcina barkeri and implications for Martian habitability

    1.Krasnopolsky, V. A., Maillard, J. P. & Owen, T. C. Detection of methane in the martian atmosphere: evidence for life?. Icarus 172, 537–547 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    2.Formisano, V., Atreya, S., Encrenaz, T., Ignatiev, N. & Giuranna, M. Detection of methane in the atmosphere of mars. Science 306, 1758–1761 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Geminale, A., Formisano, V. & Giuranna, M. Methane in Martian atmosphere: average spatial, diurnal, and seasonal behaviour. Planet. Space Sci. 56, 1194–1203 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    4.Mumma, M. J. et al. Strong release of methane on mars in northern summer 2003. Science 323, 1041–1045 (2009).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Webster, C. R. et al. Mars methane detection and variability at Gale crater. Science 347, 415–417 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Webster, C. R. et al. Background levels of methane in Mars’ atmosphere show strong seasonal variations. Science 360, 1093–1096 (2018).ADS 
    MathSciNet 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Korablev, O. et al. No detection of methane on Mars from early ExoMars Trace Gas Orbiter observations. Nature 568, 517–520 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Fries, M. et al. A cometary origin for martian atmospheric methane. Geochem. Perspect. Lett. 2, 10–23 (2016).Article 

    Google Scholar 
    9.Keppler, F. et al. Ultraviolet-radiation-induced methane emissions from meteorites and the Martian atmosphere. Nature 486, 93–96 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Moores, J. E. & Schuerger, A. C. UV degradation of accreted organics on Mars: IDP longevity, surface reservoir of organics, and relevance to the detection of methane in the atmosphere. J. Geophys. Res. Planets 117, E8 (2012).Article 
    CAS 

    Google Scholar 
    11.Schuerger, A. C., Moores, J. E., Clausen, C. A., Barlow, N. G. & Britt, D. T. Methane from UV-irradiated carbonaceous chondrites under simulated Martian conditions. J. Geophys. Res. Planets 117, E8 (2012).Article 
    CAS 

    Google Scholar 
    12.Etiope, G., Ehlmann, B. L. & Schoell, M. Low temperature production and exhalation of methane from serpentinized rocks on Earth: a potential analog for methane production on Mars. Icarus 224, 276–285 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    13.Oehler, D. Z. & Etiope, G. Methane seepage on mars: where to look and why. Astrobiology 17, 1233–1264 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Onstott, T. C. et al. Martian CH 4: sources, flux, and detection. Astrobiology 6, 377–395 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Elwood Madden, M. E., Ulrich, S. M., Onstott, T. C. & Phelps, T. J. Salinity-induced hydrate dissociation: A mechanism for recent CH4 release on Mars. Geophys. Res. Lett. https://doi.org/10.1029/2006GL029156 (2007).Article 

    Google Scholar 
    16.Conrad, R. The global methane cycle: recent advances in understanding the microbial processes involved. Environ. Microbiol. Rep. 1, 285–292 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Kendrick, M. G. & Kral, T. A. Survival of methanogens during desiccation: implications for life on mars. Astrobiology 6, 546–551 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Anderson, K. L., Apolinario, E. E. & Sowers, K. R. Desiccation as a long-term survival mechanism for the archaeon Methanosarcina barkeri. Appl. Environ. Microbiol. 78, 1473–1479 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Kral, T. A. & Altheide, S. T. Methanogen survival following exposure to desiccation, low pressure and martian regolith analogs. Planet. Space Sci. 89, 167–171 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    20.Sowers, K. R. & Gunsalus, R. P. Adaptation for growth at various saline concentrations by the archaebacterium Methanosarcina thermophila. J. Bacteriol. 170, 998–1002 (1988).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Maestrojuan, G. M. et al. Taxonomy and halotolerance of mesophilic methanosarcina strains, assignment of strains to species, and synonymy of methanosarcina mazei and methanosarcina frisia. Int. J. Syst. Bacteriol. 42, 561–567 (1992).CAS 
    Article 

    Google Scholar 
    22.Sowers, K. R., Boone, J. E. & Gunsalus, R. P. Disaggregation of methanosarcina spp and growth as single cells at elevated osmolarity. Appl. Environ. Microbiol. 59, 3832–3839 (1993).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Sowers, K. R. & Gunsalus, R. P. Halotolerance in methanosarcina spp: Role of N(sup(epsilon))-Acetyl-(beta)-Lysine, (alpha)-Glutamate, Glycine Betaine, and K(sup+) as Compatible Solutes for Osmotic Adaptation. Appl. Environ. Microbiol. 61, 4382–4388 (1995).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Roessler, M. et al. Identification of a salt-induced primary transporter for glycine betaine in the methanogen methanosarcina mazei go1. Appl. Environ. Microbiol. 68, 2133–2139 (2002).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Shcherbakova, V., Oshurkova, V. & Yoshimura, Y. The effects of perchlorates on the permafrost methanogens: implication for autotrophic life on mars. Microorganisms 3, 518–534 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Kral, T. A. et al. Sensitivity and adaptability of methanogens to perchlorates: Implications for life on Mars. Planet. Space Sci. 120, 87–95 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    27.Rivkina, E. M., Laurinavichus, K. S., Gilichinsky, D. A. & Shcherbakova, V. A. Methane generation in permafrost sediments. Dokl. Biol. Sci. https://doi.org/10.1023/A:1015366613580 (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Rivkina, E. et al. Microbial life in permafrost. Adv. Sp. Res. 33, 1215–1221 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    29.Rivkina, E. et al. Biogeochemistry of methane and methanogenic archaea in permafrost. FEMS Microbiol. Ecol. 61, 1–15 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Takai, K. et al. Cell proliferation at 122 degrees C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl. Acad. Sci. U. S. A. 105, 10949–10954 (2008).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Sinha, N., Nepal, S., Kral, T. & Kumar, P. Survivability and growth kinetics of methanogenic archaea at various pHs and pressures: implications for deep subsurface life on Mars. Planet. Space Sci. 136, 15–24 (2017).ADS 
    CAS 
    Article 

    Google Scholar 
    32.Chastain, B. K. & Kral, T. A. Approaching mars-like geochemical conditions in the laboratory: omission of artificial buffers and reductants in a study of biogenic methane production on a Smectite clay. Astrobiology 10, 889–897 (2010).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Kral, T. A., Altheide, T. S., Lueders, A. E. & Schuerger, A. C. Low pressure and desiccation effects on methanogens: Implications for life on Mars. Planet. Space Sci. 59, 264–270 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    34.Mickol, R. L. & Kral, T. A. Low pressure tolerance by methanogens in an aqueous environment: implications for subsurface life on mars. Orig. Life Evol. Biosph. 47, 511–532 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Coates, J. D. & Achenbach, L. A. Microbial perchlorate reduction: rocket-fuelled metabolism. Nat. Rev. Microbiol. 2, 569–580 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Ericksen, G. E. The Chilean Nitrate Deposits: The origin of the Chilean nitrate deposits, which contain a unique group of saline minerals, has provoked lively discussion for more than 100 years. Am. Sci. 71, 366–374 (1983).ADS 

    Google Scholar 
    37.Kounaves, S. P. et al. Discovery of natural perchlorate in the antarctic dry valleys and its global implications. Environ. Sci. Technol. 44, 2360–2364 (2010).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Hecht, M. H. et al. Detection of perchlorate and the soluble chemistry of Martian soil at the phoenix lander site. Science 325, 64–67 (2009).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    39.Navarro-González, R., Vargas, E., de la Rosa, J., Raga, A. C. & McKay, C. P. Reanalysis of the Viking results suggests perchlorate and organics at midlatitudes on Mars. J. Geophys. Res. 115, E12010 (2010).ADS 
    Article 

    Google Scholar 
    40.Glavin, D. P. et al. Evidence for perchlorates and the origin of chlorinated hydrocarbons detected by SAM at the Rocknest aeolian deposit in Gale Crater. J. Geophys. Res. Planets 118, 1955–1973 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Kounaves, S. P. et al. Identification of the perchlorate parent salts at the Phoenix Mars landing site and possible implications. Icarus 232, 226–231 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    42.Kounaves, S. P., Carrier, B. L., O’Neil, G. D., Stroble, S. T. & Claire, M. W. Evidence of martian perchlorate, chlorate, and nitrate in Mars meteorite EETA79001: Implications for oxidants and organics. Icarus 229, 206–213 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    43.Ojha, L. et al. Spectral evidence for hydrated salts in recurring slope lineae on Mars. Nat. Geosci. https://doi.org/10.1038/ngeo2546 (2015).Article 

    Google Scholar 
    44.Clark, B. C. & Kounaves, S. P. Evidence for the distribution of perchlorates on Mars. Int. J. Astrobiol. 15, 311–318 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Pestova, O. N., Myund, L. A., Khripun, M. K. & Prigaro, A. V. Polythermal study of the systems M(ClO4)2–H2O (M2+ = Mg2+, Ca2+, Sr2+, Ba2+). Russ. J. Appl. Chem. 78, 409–413 (2005).CAS 
    Article 

    Google Scholar 
    46.Chevrier, V. F., Hanley, J. & Altheide, T. S. Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site Mars. Geophys. Res. Lett. 36, L10202 (2009).ADS 
    Article 
    CAS 

    Google Scholar 
    47.Marion, G. M., Catling, D. C., Zahnle, K. J. & Claire, M. W. Modeling aqueous perchlorate chemistries with applications to Mars. Icarus 207, 675–685 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    48.Stillman, D. E. & Grimm, R. E. Dielectric signatures of adsorbed and salty liquid water at the Phoenix landing site Mars. J. Geophys. Res. 116, E09005 (2011).ADS 

    Google Scholar 
    49.Toner, J. D., Catling, D. C. & Light, B. The formation of supercooled brines, viscous liquids, and low-temperature perchlorate glasses in aqueous solutions relevant to Mars. Icarus 233, 36–47 (2014).ADS 
    CAS 
    Article 

    Google Scholar 
    50.Nikolakakos, G. & Whiteway, J. A. Laboratory investigation of perchlorate deliquescence at the surface of Mars with a Raman scattering lidar. Geophys. Res. Lett. 42, 7899–7906 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    51.Maeder, D. L. et al. The Methanosarcina barkeri Genome: Comparative Analysis with Methanosarcina acetivorans and Methanosarcina mazei Reveals Extensive Rearrangement within Methanosarcinal Genomes. J. Bacteriol. 188, 7922–7931 (2006).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Sorek, R. & Cossart, P. Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat. Rev. Genet. 11, 9–16 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    53.Lobo, A. L. & Zinder, S. H. Diazotrophy and Nitrogenase Activity in the Archaebacterium Methanosarcina barkeri 227. Appl. Environ. Microbiol. 54, 1656–1661 (1988).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Lobo, A. L. & Zinder, S. H. Nitrogenase in the archaebacterium Methanosarcina barkeri 227. J. Bacteriol. 172, 6789–6796 (1990).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Kessler, P. S. & Leigh, J. A. Genetics of nitrogen regulation in Methanococcus maripaludis. Genetics 152, 1343–1351 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Kessler, P. S., Daniel, C. & Leigh, J. A. Ammonia Switch-Off of Nitrogen Fixation in the Methanogenic Archaeon Methanococcus maripaludis: Mechanistic Features and Requirement for the Novel GlnB Homologues, NifI1 and NifI2. J. Bacteriol. 183, 882–889 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    57.Kempf, B. & Bremer, E. OpuA, an osmotically regulated binding protein-dependent transport system for the osmoprotectant glycine betaine in bacillus subtilis. J. Biol. Chem. 270, 16701–16713 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Kempf, B. & Bremer, E. Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch. Microbiol. 170, 319–330 (1998).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    59.Hoffmann, T. & Bremer, E. Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biol. Chem. 398, 193–214 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    60.Hippe, H., Caspari, D., Fiebig, K. & Gottschalk, G. Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri. Proc. Natl. Acad. Sci. 76, 494–498 (1979).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Kreisl, P. & Kandler, O. Chemical structure of the cell wall polymer of methanosarcina. Syst. Appl. Microbiol. 7, 293–299 (1986).CAS 
    Article 

    Google Scholar 
    62.Jarrell, K. F., Jones, G. M., Kandiba, L., Nair, D. B. & Eichler, J. S-layer glycoproteins and flagellins: reporters of archaeal posttranslational modifications. Archaea 2010, 1–13 (2010).Article 
    CAS 

    Google Scholar 
    63.Srinivasan, G. Pyrrolysine encoded by UAG in archaea: charging of a UAG-decoding specialized tRNA. Science 296, 1459–1462 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Bin, P., Huang, R. & Zhou, X. Oxidation resistance of the sulfur amino acids: methionine and cysteine. Biomed Res. Int. 2017, 1–6 (2017).Article 
    CAS 

    Google Scholar 
    65.Armesto, X. L., Canle, L. M., Fernández, M. I., Garcı́a, M. V. & Santaballa, J. A. First steps in the oxidation of sulfur-containing amino acids by hypohalogenation: very fast generation of intermediate sulfenyl halides and halosulfonium cations. Tetrahedron 56, 1103–1109 (2000).CAS 
    Article 

    Google Scholar 
    66.Casanueva, A., Tuffin, M., Cary, C. & Cowan, D. A. Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol. 18, 374–381 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    67.Oren, A. Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie Van Leeuwenhoek 58, 291–298 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    68.Seibel, B. A. & Walsh, P. J. Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage. J. Exp. Biol. 205, 297–306 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Lobo, A. L. & Zinder, S. H. Nitrogen fixation by methanogenic bacteria. in Biological Nitrogen Fixation (eds. Stacey, G., Burris, R. H. & Evans, H. J.) 191–211 (Chapman and Hall, 1992).70.Sohm, J. A., Webb, E. A. & Capone, D. G. Emerging patterns of marine nitrogen fixation. Nat. Rev. Microbiol. 9, 499–508 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    71.Bardiya, N. & Bae, J.-H. Dissimilatory perchlorate reduction: A review. Microbiol. Res. 166, 237–254 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Barnum, T. P. et al. Genome-resolved metagenomics identifies genetic mobility, metabolic interactions, and unexpected diversity in perchlorate-reducing communities. ISME J. 12, 1568–1581 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Oren, A., Elevi, B. R. & Mana, L. Perchlorate and halophilic prokaryotes: implications for possible halophilic life on Mars. Extremophiles 18, 75–80 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    74.Liebensteiner, M. G., Pinkse, M. W. H., Schaap, P. J., Stams, A. J. M. & Lomans, B. P. Archaeal (Per)Chlorate reduction at high temperature: an interplay of biotic and abiotic reactions. Science 340, 85–87 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    75.Bender, K. S. et al. Identification, characterization, and classification of genes encoding perchlorate reductase. J. Bacteriol. 187, 5090–5096 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.Youngblut, M. D. et al. Perchlorate reductase is distinguished by active site aromatic gate residues. J. Biol. Chem. 291, 9190–9202 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Okeke, B. C., Giblin, T. & Frankenberger, W. T. Reduction of perchlorate and nitrate by salt tolerant bacteria. Environ. Pollut. https://doi.org/10.1016/S0269-7491(01)00288-3 (2002).Article 
    PubMed 

    Google Scholar 
    78.He, L. et al. Biological perchlorate reduction: which electron donor we can choose?. Environ. Sci. Pollut. Res. 26, 16906–16922 (2019).CAS 
    Article 

    Google Scholar 
    79.Xie, T. et al. Perchlorate bioreduction linked to methane oxidation in a membrane biofilm reactor: performance and microbial community structure. J. Hazard. Mater. https://doi.org/10.1016/j.jhazmat.2018.06.011 (2018).Article 
    PubMed 

    Google Scholar 
    80.Chaudhuri, S. K., O’Connor, S. M., Gustavson, R. L., Achenbach, L. A. & Coates, J. D. Environmental factors that control microbial perchlorate reduction. Appl. Environ. Microbiol. https://doi.org/10.1128/AEM.68.9.4425-4430.2002 (2002).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    81.Abu-Omar, M. M. Effective and catalytic reduction of perchlorate by atom transfer-reaction kinetics and mechanisms. Comments Inorg. Chem. 24, 15–37 (2003).CAS 
    Article 

    Google Scholar 
    82.Adkins, H. & Cramer, H. I. The use of nickel as a catalyst for hydrogenation. J. Am. Chem. Soc. 52, 4349–4358 (1930).CAS 
    Article 

    Google Scholar 
    83.Thauer, R. K. et al. Hydrogenases from methanogenic archaea, nickel, a novel cofactor, and H2 storage. Annu. Rev. Biochem. 79, 507–536 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Zhang, H., Bruns, M. A. & Logan, B. E. Perchlorate reduction by a novel chemolithoautotrophic, hydrogen-oxidizing bacterium. Environ. Microbiol. https://doi.org/10.1046/j.1462-2920.2002.00338.x (2002).Article 
    PubMed 

    Google Scholar 
    85.Ide, T., Bäumer, S. & Deppenmeier, U. Energy conservation by the H2: heterodisulfide oxidoreductase from methanosarcina mazei Gö1: identification of two proton-translocating segments. J. Bacteriol. 181, 4076–4080 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Deppenmeier, U. The membrane-bound electron transport system of methanosarcina species. J. Bioenerg. Biomembr. 36, 55–64 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Meuer, J., Kuettner, H. C., Zhang, J. K., Hedderich, R. & Metcalf, W. W. Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc. Natl. Acad. Sci. 99, 5632–5637 (2002).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    88.Kulkarni, G., Mand, T. D. & Metcalf, W. W. Energy Conservation via Hydrogen Cycling in the Methanogenic Archaeon Methanosarcina barkeri. MBio 9, (2018).89.Bobik, T. Formyl-methanofuran synthesis in Methanobacterium thermoautotrophicum. FEMS Microbiol. Lett. 87, 323–326 (1990).CAS 
    Article 

    Google Scholar 
    90.Wang, D. M., Shah, S. I., Chen, J. G. & Huang, C. P. Catalytic reduction of perchlorate by H2 gas in dilute aqueous solutions. Sep. Purif. Technol. 60, 14–21 (2008).CAS 
    Article 

    Google Scholar 
    91.Thauer, R. K., Kaster, A.-K., Seedorf, H., Buckel, W. & Hedderich, R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6, 579–591 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    92.Mand, T. D. & Metcalf, W. W. Energy Conservation and Hydrogenase Function in Methanogenic Archaea, in Particular the Genus Methanosarcina. Microbiol. Mol. Biol. Rev. 83, (2019).93.Rummel, J. D. et al. A new analysis of mars “special regions”: findings of the second MEPAG special regions science analysis group (SR-SAG2). Astrobiology 14, 887–968 (2014).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    94.Bryant, M. P. & Boone, D. R. Emended description of strain MST(DSM 800T), the type strain of methanosarcina barkeri. Int. J. Syst. Bacteriol. 37, 169–170 (1987).Article 

    Google Scholar 
    95.Widdel, F., Kohring, G.-W. & Mayer, F. Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. Arch. Microbiol. 134, 286–294 (1983).CAS 
    Article 

    Google Scholar 
    96.Francisco, D. E., Mah, R. A. & Rabin, A. C. Acridine orange-epifluorescence technique for counting bacteria in natural waters. Trans. Am. Microsc. Soc. 92, 416 (1973).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    97.Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    98.Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    99.Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    100.Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    101.Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinformatics 10, 421 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    102.Love, M., Anders, S. & Huber, W. Differential analysis of count data–the DESeq2 package. Genome Biol. 15, 10–1186 (2014).Article 
    CAS 

    Google Scholar 
    103.Ogata, H. et al. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 27, 29–34 (1999).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish

    1.Clobert, J., Baguette, M., Benton, T. G. & Bullock, J. M. Dispersal Ecology and Evolution (Oxford University Press, 2012).Book 

    Google Scholar 
    2.Paris, C. B. & Cowen, R. K. Direct evidence of a biophysical retention mechanism for coral reef fish larvae. Limnol. Oceanogr. 49, 1964–1979 (2004).ADS 
    Article 

    Google Scholar 
    3.Roberts, C. M. Connectivity and management of Caribbean coral reefs. Science 278, 1454–1457 (1997).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Fisher, R. & Wilson, S. K. Maximum sustainable swimming speeds of late-stage larvae of nine species of reef fishes. J. Exp. Mar. Biol. Ecol. 312, 171–186 (2004).Article 

    Google Scholar 
    5.Fisher, R., Leis, J. M., Clark, D. L. & Wilson, S. K. Critical swimming speeds of late-stage coral reef fish larvae: variation within species, among species and between locations. Mar. Biol. 147, 1201–1212 (2005).Article 

    Google Scholar 
    6.Leis, J. M. Ontogeny of behaviour in larvae of marine demersal fishes. Ichthyol. Res. 57, 325–342 (2010).Article 

    Google Scholar 
    7.Faillettaz, R., Durand, E., Paris, C. B., Koubbi, P. & Irisson, J.-O. Swimming speeds of Mediterranean settlement-stage fish larvae nuance Hjort’s aberrant drift hypothesis. Limnol. Oceanogr. 63, 509–523 (2018).ADS 
    Article 

    Google Scholar 
    8.Majoris, J. E., Catalano, K. A., Scolaro, D., Atema, J. & Buston, P. M. Ontogeny of larval swimming abilities in three species of coral reef fishes and a hypothesis for their impact on the spatial scale of dispersal. Mar. Biol. 166, 159 (2019).Article 

    Google Scholar 
    9.Leis, J. M., Sweatman, H. P. & Reader, S. E. What the pelagic stages of coral reef fishes are doing out in blue water: daytime field observations of larval behavioural capabilities. Mar. Freshw. Res. 47, 401–411 (1996).Article 

    Google Scholar 
    10.Leis, J., Paris, C., Irisson, J., Yerman, M. & Siebeck, U. Orientation of fish larvae in situ is consistent among locations, years and methods, but varies with time of day. Mar. Ecol. Prog. Ser. 505, 193–208 (2014).ADS 
    Article 

    Google Scholar 
    11.Leis, J. M. & Carson-Ewart, B. M. Orientation of pelagic larvae of coral-reef fishes in the ocean. Mar. Ecol. Prog. Ser. 252, 239–253 (2003).ADS 
    Article 

    Google Scholar 
    12.Paris, C. B., Guigand, C. M., Irisson, J.-O., Fisher, R. & D’Alessandro, E. Orientation with no frame of reference (OWNFOR): a novel system to observe and quantify orientation in reef fish larvae. In Caribbean Connectivity: Implications for Marine Protected Area Management 52–62 (2008).13.Rossi, A., Irisson, J.-O., Levaray, M., Pasqualini, V. & Agostini, S. Orientation of Mediterranean fish larvae varies with location. Mar. Biol. 166, 100 (2019).Article 

    Google Scholar 
    14.Simpson, S. D., Meekan, M., Montgomery, J., McCauley, R. & Jeffs, A. Homeward sound. Science 308, 221–221 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Leis, J. M., Siebeck, U. & Dixson, D. L. How nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes. Integr. Comp. Biol. 51, 826–843 (2011).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Paris, C. B. et al. Reef odor: a wake up call for navigation in reef fish larvae. PLoS ONE 8, e72808 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Mouritsen, H., Atema, J., Kingsford, M. J. & Gerlach, G. Sun compass orientation helps coral reef fish larvae return to their natal reef. PLoS ONE 8, e66039 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Berenshtein, I. et al. Polarized light sensitivity and orientation in coral reef fish post-larvae. PLoS ONE 9, e88468 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    19.Bottesch, M. et al. A magnetic compass that might help coral reef fish larvae return to their natal reef. Curr. Biol. 26, R1266–R1267 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Cresci, A., Allan, B. J. M., Shema, S. D., Skiftesvik, A. B. & Browman, H. I. Orientation behavior and swimming speed of Atlantic herring larvae (Clupea harengus) in situ and in laboratory exposures to rotated artificial magnetic fields. J. Exp. Mar. Biol. Ecol. 526, 151358 (2020).Article 

    Google Scholar 
    21.Faillettaz, R., Paris, C. B. & Irisson, J.-O. Larval fish swimming behavior alters dispersal patterns from marine protected areas in the North-Western Mediterranean Sea. Front. Mar. Sci. 5, 97 (2018).Article 

    Google Scholar 
    22.Staaterman, E., Paris, C. B. & Helgers, J. Orientation behavior in fish larvae: a missing piece to Hjort’s critical period hypothesis. J. Theor. Biol. 304, 188–196 (2012).PubMed 
    MATH 
    Article 
    PubMed Central 

    Google Scholar 
    23.Lara, M. R. Development of the nasal olfactory organs in the larvae, settlement-stages and some adults of 14 species of Caribbean reef fishes (Labridae, Scaridae, Pomacentridae). Mar. Biol. 154, 51–64 (2008).Article 

    Google Scholar 
    24.Arvedlund, M. & Kavanagh, K. The senses and environmental cues used by marine larvae of fish and decapod crustaceans to find tropical coastal ecosystems. In Ecological Connectivity among Tropical Coastal Ecosystems (ed. Nagelkerken, I.) 135–184 (Springer, 2009).Chapter 

    Google Scholar 
    25.Teodósio, M. A., Paris, C. B., Wolanski, E. & Morais, P. Biophysical processes leading to the ingress of temperate fish larvae into estuarine nursery areas: a review. Estuar. Coast. Shelf Sci. 183, 187–202 (2016).ADS 
    Article 

    Google Scholar 
    26.Hu, Y., Majoris, J. E., Buston, P. M. & Webb, J. F. Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology. J. Fish Biol. 95, 311–323 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Nickles, K. R., Hu, Y., Majoris, J. E., Buston, P. M. & Webb, J. F. Organization and ontogeny of a complex lateral line system in a Goby (Elacatinus lori), with a consideration of function and ecology. Copeia 108, 863–885 (2020).Article 

    Google Scholar 
    28.Fuiman, L., Higgs, D. & Poling, K. Changing structure and function of the ear and lateral line system of fishes during development. Am. Fish. Soc. Symp. 2004, 117–144 (2004).
    Google Scholar 
    29.Blaxter, J. H. S. Light intensity, vision, and feeding in young plaice. J. Exp. Mar. Biol. Ecol. 2, 293–307 (1968).Article 

    Google Scholar 
    30.Blaxter, J. H. S. & Hoss, D. E. The effect of rapid changes of hydrostatic pressure on the Atlantic herring Clupea harengus L. II. The response of the auditory bulla system in larvae and juveniles. J. Exp. Mar. Biol. Ecol. 41, 87–100 (1979).Article 

    Google Scholar 
    31.Colin, P. L. A new species of sponge-dwelling Elacatinus (Pisces: Gobiidae) from the western Caribbean. Zootaxa 106, 1–7 (2002).Article 

    Google Scholar 
    32.Colin, P. L. Fishes as living tracers of connectivity in the tropical western North Atlantic: I. Distribution of the neon gobies, genus Elacatinus (Pisces: Gobiidae). Zootaxa 2370, 36–52 (2010).Article 

    Google Scholar 
    33.Brandl, S. J. et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science 364, 1189–1192 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.D’Aloia, C. C., Majoris, J. E. & Buston, P. M. Predictors of the distribution and abundance of a tube sponge and its resident goby. Coral Reefs 30, 777 (2011).ADS 
    Article 

    Google Scholar 
    35.Majoris, J. E., Francisco, F. A., Atema, J. & Buston, P. M. Reproduction, early development, and larval rearing strategies for two sponge-dwelling neon gobies, Elacatinus lori and E. colini. Aquaculture 483, 286–295 (2018).Article 

    Google Scholar 
    36.D’Aloia, C. C. et al. Patterns, causes, and consequences of marine larval dispersal. Proc. Natl. Acad. Sci. 112, 13940–13945 (2015).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    37.Majoris, J. E., D’Aloia, C. C., Francis, R. K. & Buston, P. M. Differential persistence favors habitat preferences that determine the distribution of a reef fish. Behav. Ecol. 29, 429–439 (2018).Article 

    Google Scholar 
    38.Chaput, R., Majoris, J. E., Guigand, C. M., Huse, M. & D’Alessandro, E. K. Environmental conditions and paternal care determine hatching synchronicity of coral reef fish larvae. Mar. Biol. 166, 118 (2019).Article 
    CAS 

    Google Scholar 
    39.D’Aloia, C., Xuereb, A., Fortin, M., Bogdanowicz, S. & Buston, P. Limited dispersal explains the spatial distribution of siblings in a reef fish population. Mar. Ecol. Prog. Ser. 607, 143–154 (2018).ADS 
    Article 

    Google Scholar 
    40.Williamson, D. H. et al. Large-scale, multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park. Mol. Ecol. 25, 6039–6054 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Almany, G. R. et al. Larval fish dispersal in a coral-reef seascape. Nat. Ecol. Evol. 1, 0148 (2017).Article 

    Google Scholar 
    42.Bode, M. et al. Successful validation of a larval dispersal model using genetic parentage data. PLOS Biol. 17, e3000380 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Nakae, M., Asaoka, R., Wada, H. & Sasaki, K. Fluorescent dye staining of neuromasts in live fishes: an aid to systematic studies. Ichthyol. Res. 59, 286–290 (2012).Article 

    Google Scholar 
    44.Webb, J. F. & Shirey, J. E. Postembryonic development of the cranial lateral line canals and neuromasts in zebrafish. Dev. Dyn. 228, 370–385 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Becker, E. A., Bird, N. C. & Webb, J. F. Post-embryonic development of canal and superficial neuromasts and the generation of two cranial lateral line phenotypes. J. Morphol. 277, 1273–1291 (2016).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Webb, J. F. Morphological diversity, development, and evolution of the mechanosensory lateral line system. In The Lateral Line System (eds Coombs, S. et al.) 17–72 (Springer, 2014). https://doi.org/10.1007/2506_2013_12.Chapter 

    Google Scholar 
    47.Asaoka, R., Nakae, M. & Sasaki, K. The innervation and adaptive significance of extensively distributed neuromasts in Glossogobius olivaceus (Perciformes: Gobiidae). Ichthyol. Res. 59, 143–150 (2011).Article 

    Google Scholar 
    48.Asaoka, R., Nakae, M. & Sasaki, K. Innervation of the lateral line system in Rhyacichthys aspro: the origin of superficial neuromast rows in gobioids (Perciformes: Rhyacichthyidae). Ichthyol. Res. 61, 49–58 (2014).Article 

    Google Scholar 
    49.Nickles, K. Ontogeny of the lateral line and visual systems of a Caribbean Reef Goby, Elacatinus lori (University of Rhode Island, 2019).50.Shand, J., Døving, K. B. & Collin, S. P. Optics of the developing fish eye: comparisons of Matthiessen’s ratio and the focal length of the lens in the black bream Acanthopagrus butcheri (Sparidae, Teleostei). Vis. Res. 39, 1071–1078 (1999).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Webb, J. F. et al. Development of the ear, hearing capabilities and laterophysic connection in the spotfin butterflyfish (Chaetodon ocellatus). Environ. Biol. Fishes 95, 275–290 (2012).Article 

    Google Scholar 
    52.Popper, A. N. & Hoxter, B. Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation. Hear. Res. 15, 133–142 (1984).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Bever, M. M. & Fekete, D. M. Atlas of the developing inner ear in zebrafish. Dev. Dyn. 223, 536–543 (2002).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Haddon, C. & Lewis, J. Early ear development in the embryo of the Zebrafish, Danio rerio. J. Comp. Neurol. 365, 113–128 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Kawamura, G. et al. Morphogenesis of sense organs in the bluefin tuna Thunnus orientalis. in The Big Fish Bang Proceedings of the 26th Annual Larval Fish Conference (eds Browman, H. & Skiftesvik, A. B.) 123–135 (2003).
    Google Scholar 
    56.Pankhurst, P. M. & Butler, P. Development of the sensory organs in the greenback flounder, Rhombosolea tapirina. Mar. Freshw. Behav. Physiol. 28, 55–73 (1996).Article 

    Google Scholar 
    57.Lara, M. R. Morphology of the eye and visual acuities in the settlement-intervals of some Coral Reef Fishes (Labridae, Scaridae). Environ. Biol. Fishes 62, 365–378 (2001).Article 

    Google Scholar 
    58.Lara, M. R. Sensory Development in Settlement-Stage Larvae of Caribbean Labrids and Scarids: A Comparative Study with Implications for Ecomorphology and Life History Strategies (College of William and Mary, 1999).
    Google Scholar 
    59.Lecchini, D., Planes, S. & Galzin, R. Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat. Behav. Ecol. Sociobiol. 58, 18–26 (2005).Article 

    Google Scholar 
    60.Dixson, D. L. et al. Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish. Oecologia 174, 99–107 (2014).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Irisson, J.-O., Guigand, C. & Paris, C. B. Detection and quantification of marine larvae orientation in the pelagic environment. Limnol. Oceanogr. Methods 7, 664–672 (2009).Article 

    Google Scholar 
    62.Irisson, J.-O., Paris, C. B., Leis, J. M. & Yerman, M. N. With a little help from my friends: group orientation by larvae of a coral reef fish. PLoS ONE 10, e0144060 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    63.Faillettaz, R., Blandin, A., Paris, C. B., Koubbi, P. & Irisson, J.-O. Sun-compass orientation in Mediterranean fish larvae. PLoS ONE 10, e0135213 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    64.Lindo-Atichati, D., Curcic, M., Paris, C. B. & Buston, P. M. Description of surface transport in the region of the Belizean Barrier Reef based on observations and alternative high-resolution models. Ocean Model 106, 74–89 (2016).ADS 
    Article 

    Google Scholar 
    65.Agostinelli, C. & Lund, U. R package ‘circular’: Circular Statistics (version 0.4-93). https://r-forge.r-project.org/projects/circular/ (2017).66.R Core Team. R: A language and environment for statistical computing (R Found Stat Comput, 2013).
    Google Scholar 
    67.Leis, J., Hay, A. & Howarth, G. Ontogeny of in situ behaviours relevant to dispersal and population connectivity in larvae of coral-reef fishes. Mar. Ecol. Prog. Ser. 379, 163–179 (2009).ADS 
    Article 

    Google Scholar 
    68.Leis, J. M. & Carson-Ewart, B. M. (eds) The larvae of Indo-Pacific coastal fishes: an identification guide to marine fish larvae, 2nd edn. (Brill, 2004).
    Google Scholar 
    69.Kingsford, M. J. et al. Sensory environments, larval abilities and local self-recruitment. Bull. Mar. Sci. 70, 309–340 (2002).
    Google Scholar 
    70.Cresci, A. et al. Atlantic haddock (Melanogrammus aeglefinus) larvae have a magnetic compass that guides their orientation. iScience 19, 1173–1178 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl. Acad. Sci. 104, 858–863 (2007).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Dixson, D. L. et al. Coral reef fish smell leaves to find island homes. Proc. R. Soc. B Biol. Sci. 275, 2831–2839 (2008).Article 

    Google Scholar 
    73.Berenshtein, I. et al. Auto-correlated directional swimming can enhance settlement success and connectivity in fish larvae. J. Theor. Biol. 439, 76–85 (2018).MathSciNet 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Shaw, A. K., D’Aloia, C. C. & Buston, P. M. The evolution of marine larval dispersal kernels in spatially structured habitats: analytical models, individual-based simulations, and comparisons with empirical estimates. Am. Nat. 193, 424–435 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Gross, M. R. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11, 92–98 (1996).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Ronce, O. & Clobert, J. Dispersal syndromes. In Dispersal Ecology and Evolution Vol. 55 (eds Clobert, J. et al.) 119–138 (Oxford University Press, Oxford, 2012).Chapter 

    Google Scholar 
    77.Huebert, K. & Sponaugle, S. Observed and simulated swimming trajectories of late-stage coral reef fish larvae off the Florida Keys. Aquat. Biol. 7, 207–216 (2009).Article 

    Google Scholar 
    78.Hamilton, W. D. & May, R. M. Dispersal in stable habitats. Nature 269, 578–581 (1977).ADS 
    Article 

    Google Scholar 
    79.Leis, J. et al. In situ orientation of fish larvae can vary among regions. Mar. Ecol. Prog. Ser. 537, 191–203 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    80.Botsford, L. W. et al. Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28, 327–337 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.White, J. W., Botsford, L. W., Hastings, A. & Largier, J. L. Population persistence in marine reserve networks: incorporating spatial heterogeneities in larval dispersal. Mar. Ecol. Prog. Ser. 398, 49–67 (2010).ADS 
    Article 

    Google Scholar 
    82.Green, A. L. et al. Larval dispersal and movement patterns of coral reef fishes, and implications for marine reserve network design: connectivity and marine reserves. Biol. Rev. https://doi.org/10.1111/brv.12155 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    83.Munguia-Vega, A. et al. Ecological guidelines for designing networks of marine reserves in the unique biophysical environment of the Gulf of California. Rev. Fish Biol. Fish. 28, 749–776 (2018).Article 

    Google Scholar 
    84.Cowen, R. K., Paris, C. B. & Srinivasan, A. Scaling of connectivity in marine populations. Science 311, 522–527 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    85.Paris, C. B., Chérubin, L. M. & Cowen, R. K. Surfing, spinning, or diving from reef to reef: effects on population connectivity. Mar. Ecol. Prog. Ser. 347, 285–300 (2007).ADS 
    Article 

    Google Scholar 
    86.Mann, D. A., Casper, B. M., Boyle, K. S. & Tricas, T. C. On the attraction of larval fishes to reef sounds. Mar. Ecol. Prog. Ser. 338, 307–310 (2007).ADS 
    Article 

    Google Scholar 
    87.Esri. World Imagery [basemap]. 500m. Imagery, basemaps, and land cover. May 14, 2020. https://www.arcgis.com/home/webmap/viewer.html. (2020). More

  • in

    Short term fluctuating temperature alleviates Daphnia stoichiometric constraints

    1.Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).Article 

    Google Scholar 
    2.Dillon, M. E., Wang, G. & Huey, R. B. Global metabolic impacts of recent climate warming. Nature 467, 704–706. https://doi.org/10.1038/nature09407 (2010).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    3.Elser, J. J. et al. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 3, 540–550 (2000).Article 

    Google Scholar 
    4.Elser, J., Obrien, W., Dobberfuhl, D. & Dowling, T. The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats. J. Evol. Biol. 13, 845–853 (2000).Article 

    Google Scholar 
    5.Hessen, D. O., Elser, J. J., Sterner, R. W. & Urabe, J. Ecological stoichiometry: An elementary approach using basic principles. Limnol. Oceanogr. 58, 2219–2236 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    6.Hessen, D. O., Faerovig, P. J. & Andersen, T. Light, nutrients, and P : C ratios in algae: Grazer performance related to food quality and quantity. Ecology 83, 1886–1898 (2002).Article 

    Google Scholar 
    7.Moody, E. K., Rugenski, A. T., Sabo, J. L., Turner, B. L. & Elser, J. J. Does the growth rate hypothesis apply across temperatures? Variation in the growth rate and body phosphorus of neotropical benthic grazers. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2017.00014 (2017).Article 

    Google Scholar 
    8.Prater, C., Wagner, N. D. & Frost, P. C. Seasonal effects of food quality and temperature on body stoichiometry, biochemistry, and biomass production in Daphnia populations. Limnol. Oceanogr. 63, 1727–1740. https://doi.org/10.1002/lno.10803 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    9.Boersma, M. et al. Temperature driven changes in the diet preference of omnivorous copepods: No more meat when it’s hot?. Ecol. Lett. 19, 45–53. https://doi.org/10.1111/ele.12541 (2016).Article 
    PubMed 

    Google Scholar 
    10.Wojewodzic, M. W., Kyle, M., Elser, J. J., Hessen, D. O. & Andersen, T. Joint effect of phosphorus limitation and temperature on alkaline phosphatase activity and somatic growth in Daphnia magna. Oecologia 165, 837–846. https://doi.org/10.1007/s00442-010-1863-2 (2011).ADS 
    Article 
    PubMed 

    Google Scholar 
    11.Starke, C. W. E., Jones, C. L. C., Burr, W. S. & Frost, P. C. Interactive effects of water temperature and stoichiometric food quality on Daphnia pulicaria. Freshwat. Biol. 66, 256–265. https://doi.org/10.1111/fwb.13633 (2020).CAS 
    Article 

    Google Scholar 
    12.Ruiz, T. et al. U-shaped response Unifies views on temperature dependency of stoichiometric requirements. Ecol. Lett. 23, 860–869. https://doi.org/10.1111/ele.13493 (2020).Article 
    PubMed 

    Google Scholar 
    13.Persson, J., Wojewodzic, M. W., Hessen, D. O. & Andersen, T. Increased risk of phosphorus limitation at higher temperatures for Daphnia magna. Oecologia 165, 123–129. https://doi.org/10.1007/s00442-010-1756-4 (2011).ADS 
    Article 
    PubMed 

    Google Scholar 
    14.Malzahn, A. M., Doerfler, D. & Boersma, M. Junk food gets healthier when it’s warm. Limnol. Oceanogr. 61, 1677–1685. https://doi.org/10.1002/lno.10330 (2016).ADS 
    Article 

    Google Scholar 
    15.Cross, W. F., Hood, J. M., Benstead, J. P., Huryn, A. D. & Nelson, D. Interactions between temperature and nutrients across levels of ecological organization. Glob. Change Biol. 21, 1025–1040. https://doi.org/10.1111/gcb.12809 (2015).ADS 
    Article 

    Google Scholar 
    16.Woods, H. A. et al. Temperature and the chemical composition of poikilothermic organisms. Funct. Ecol. 17, 237–245. https://doi.org/10.1046/j.1365-2435.2003.00724.x (2003).Article 

    Google Scholar 
    17.Cotner, J. B., Makino, W. & Biddanda, B. A. Temperature affects stoichiometry and biochemical composition of Escherichia coli. Microb. Ecol. 52, 26–33. https://doi.org/10.1007/s00248-006-9040-1 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    18.Hessen, D. O. et al. Changes in stoichiometry, cellular RNA, and alkaline phosphatase activity of Chlamydomonas in response to temperature and nutrients. Front. Microbiol. 8, 18. https://doi.org/10.3389/fmicb.2017.00018 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Van Geest, G. J., Sachse, R., Brehm, M., van Donk, E. & Hessen, D. Maximizing growth rate at low temperatures: RNA:DNA allocation strategies and life history traits of Arctic and temperate Daphnia. Polar Biol. 33, 1255–1262 (2010).Article 

    Google Scholar 
    20.Prater, C., Wagner, N. D. & Frost, P. C. Interactive effects of genotype and food quality on consumer growth rate and elemental content. Ecology 98, 1399–1408. https://doi.org/10.1002/ecy.1795 (2017).Article 
    PubMed 

    Google Scholar 
    21.Lampert, W. The adaptive significance of diel vertical migration of zooplankton. Funct. Ecol. 3, 21–27 (1989).Article 

    Google Scholar 
    22.Williamson, C. E., Fischer, J. M., Bollens, S. M., Overholt, E. P. & Breckenridge, J. K. Towards a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm. Limnol. Oceanogr. 56, 1603–1623 (2011).ADS 
    Article 

    Google Scholar 
    23.Dawidowicz, P. & Loose, C. J. Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol. Oceanogr. 37, 1589–1595 (1992).ADS 
    Article 

    Google Scholar 
    24.Mikulski, A., Grzesiuk, M., Rakowska, A., Bernatowicz, P. & Pijanowska, J. Thermal shock in Daphnia: cost of diel vertical migrations or inhabiting thermally-unstable waterbodies?. Fund. Appl. Limnol. 190, 213–220. https://doi.org/10.1127/fal/2017/0989 (2017).Article 

    Google Scholar 
    25.Reichwaldt, E. S., Wolf, I. D. & Stibor, H. Effects of a fluctuating temperature regime experienced by Daphnia during diel vertical migration on Daphnia life history parameters. Hydrobiologia 543, 199–205. https://doi.org/10.1007/s10750-004-7451-x (2005).Article 

    Google Scholar 
    26.Orcutt, J. D. & Porter, K. G. Diel vertical migration in zooplankton. Constant and fluctuating temperature effects on life history parameters of Daphnia. Limnol. Oceanogr. 28, 720–730 (1983).ADS 
    Article 

    Google Scholar 
    27.Stich, H. B. & Lampert, W. Growth and reproduction of migrating and non-migrating Daphnia species under simulated food and temperature conditions of diurnal vertical migration. Oecologia 61, 192–196. https://doi.org/10.1007/BF00396759 (1984).ADS 
    Article 
    PubMed 

    Google Scholar 
    28.Fischer, J. M. et al. Diel vertical migration of copepods in mountain lakes: The changing role of ultraviolet radiation across a transparency gradient. Limnol. Oceanogr. 60, 252–262. https://doi.org/10.1002/lno.10019 (2015).ADS 
    Article 

    Google Scholar 
    29.Kessler, K., Lockwood, R. S., Williamson, C. E. & Saros, J. E. Vertical distribution of zooplankton in subalpine and alpine lakes: Ultraviolet radiation, fish predation, and the transparency-gradient hypothesis. Limnol. Oceanogr. 53, 2374–2382 (2008).ADS 
    Article 

    Google Scholar 
    30.Bergström, A.-K., Karlsson, J., Karlsson, D. & Vrede, T. Contrasting plankton stoichiometry and nutrient regeneration in northern arctic and boreal lakes. Aquat. Sci. https://doi.org/10.1007/s00027-018-0575-2 (2018).Article 

    Google Scholar 
    31.Sterner, R. W. On the phosphorus limitation paradigm for lakes. Int. Rev. Hydrobiol. 93, 433–445. https://doi.org/10.1002/iroh.200811068 (2008).CAS 
    Article 

    Google Scholar 
    32.Sterner, R. W. C: N: P stoichiometry in Lake superior: Freshwater sea as end member. Inland Waters 1, 29–46 (2011).CAS 
    Article 

    Google Scholar 
    33.Modenutti, B. E. et al. Environmental changes affecting light climate in oligotrophic mountain lakes: The deep chlorophyll maxima as a sensitive variable. Aquat. Sci. 75, 361–371. https://doi.org/10.1007/s00027-012-0282-3 (2013).CAS 
    Article 

    Google Scholar 
    34.Longhi, M. L. & Beisner, B. E. Environmental factors controlling the vertical distribution of phytoplankton in lakes. J. Plankton Res. 31, 1195–1207. https://doi.org/10.1093/plankt/fbp065 (2009).CAS 
    Article 

    Google Scholar 
    35.Leach, T. H. et al. Patterns and drivers of deep chlorophyll maxima structure in 100 lakes: The relative importance of light and thermal stratification. Limnol. Oceanogr. 63, 628–646. https://doi.org/10.1002/lno.10656 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    36.Laspoumaderes, C. et al. Glacier melting and stoichiometric implications for lake community structure: Zooplankton species distributions across a natural light gradient. Glob. Change Biol. 19, 316–326. https://doi.org/10.1111/gcb.12040 (2013).ADS 
    Article 

    Google Scholar 
    37.Jacobs, A. F. G., Jetten, T. H., Lucassen, D., Heusinkveld, B. G. & Joost, P. N. Diurnal temperature fluctuations in a natural shallow water body. Agric. For. Meteorol. 88, 269–277. https://doi.org/10.1016/S0168-1923(97)00039-7 (1997).ADS 
    Article 

    Google Scholar 
    38.Vilas, M. P., Marti, C. L., Adams, M. P., Oldham, C. E. & Hipsey, M. R. Invasive macrophytes control the spatial and temporal patterns of temperature and dissolved oxygen in a shallow lake: A proposed feedback mechanism of macrophyte loss. Front. Plant Sci. 8, 2097. https://doi.org/10.3389/fpls.2017.02097 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Burks, R. L., Lodge, D. M., Jeppesen, E. & Lauridsen, T. L. Diel horizontal migration of zooplankton: Costs and benefits of inhabiting the littoral. Freshwat. Biol. 47, 343–365 (2002).Article 

    Google Scholar 
    40.Morris, D. P. et al. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol. Oceanogr. 40, 1381–1391 (1995).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Balseiro, E. G., Modenutti, B. E., Queimaliños, C. & Reissig, M. Daphnia distribution in Andean Patagonian lakes: Effect of low food quality and fish predation. Aquat. Ecol. 41, 599–609 (2007).CAS 
    Article 

    Google Scholar 
    42.Modenutti, B. E., Wolinski, L., Souza, M. S. & Balseiro, E. G. When eating a prey is risky: Implications for predator diel vertical migration. Limnol. Oceanogr. 63, 939–950. https://doi.org/10.1002/lno.10681 (2018).ADS 
    Article 

    Google Scholar 
    43.Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Effects of size and temperature on developmental time. Nature 417, 70–73. https://doi.org/10.1038/417070a (2002).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    44.Acharya, K., Kyle, M. & Elser, J. J. Biological stoichiometry of Daphnia growth: An ecophysiological test of the growth rate hypothesis. Limnol. Oceanogr. 49, 656–665 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    45.Souza, M. S., Hansson, L.-A., Hylander, S., Modenutti, B. E. & Balseiro, E. G. Rapid enzymatic response to compensate UV radiation in copepods. PLoS ONE 7, e32046. https://doi.org/10.1371/journal.pone.0032046 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Wolinski, L., Modenutti, B., Souza, M. S. & Balseiro, E. Interactive effects of temperature, ultraviolet radiation and food quality on zooplankton alkaline phosphatase activity. Environ. Pollut. 213, 135–142. https://doi.org/10.1016/j.envpol.2016.02.016 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    47.Xie, J. et al. Physiological effects of compensatory growth during the larval stage of the ladybird Cryptolaemus montrouzieri. J. Insect Physiol. 83, 37–42. https://doi.org/10.1016/j.jinsphys.2015.11.001 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    48.Dmitriew, C. & Rowe, L. Resource limitation, predation risk and compensatory growth in a damselfly. Oecologia 142, 150–154. https://doi.org/10.1007/s00442-004-1712-2 (2005).ADS 
    Article 
    PubMed 

    Google Scholar 
    49.Malzahn, A. M. & Boersma, M. Effects of poor food quality on copepod growth are dose dependent and non-reversible. Oikos 121, 1408–1416. https://doi.org/10.1111/j.1600-0706.2011.20186.x (2012).Article 

    Google Scholar 
    50.Droop, M. R. Some thoughts on nutrient limitation in algae. J. PhycoI. 9, 264–272 (1973).CAS 
    Article 

    Google Scholar 
    51.Boersma, M. The nutritional quality of P-limited algae for Daphnia. Limnol. Oceanogr. 45, 1157–1161 (2000).ADS 
    CAS 
    Article 

    Google Scholar 
    52.Plath, K. & Boersma, M. Mineral limitation of zooplankton: Stoichiometric constraints and optimal foraging. Ecology 82, 1260–1269 (2001).Article 

    Google Scholar 
    53.Barbiero, R. P. & Tuchman, M. L. Results from the US EPA’s biological open water surveillance program of the Laurentian Great Lakes: II. Deep chlorophyll maxima. J. Great Lakes Res. 27, 155–166 (2001).CAS 
    Article 

    Google Scholar 
    54.Camacho, A. On the occurrence and ecological features of deep chlorophyll maxima (DCM) in Spanish stratified lakes. Limnetica 25, 453–478 (2006).
    Google Scholar 
    55.Pérez, G. L., Queimaliños, C. P. & Modenutti, B. E. Light climate and plankton in the deep chlorophyll maxima in North Patagonian Andean lakes. J. Plankton Res. 24, 591–599 (2002).Article 

    Google Scholar 
    56.Magee, M. R. & Wu, C. H. Response of water temperatures and stratification to changing climate in three lakes with different morphometry. Hydrol. Earth Syst. Sci. 21, 6253–6274. https://doi.org/10.5194/hess-21-6253-2017 (2017).ADS 
    Article 

    Google Scholar 
    57.Niedrist, G. H., Psenner, R. & Sommaruga, R. Climate warming increases vertical and seasonal water temperature differences and inter-annual variability in a mountain lake. Clim. Change 151, 473–490. https://doi.org/10.1007/s10584-018-2328-6 (2018).ADS 
    Article 

    Google Scholar 
    58.Kilham, S. S., Kreeger, D. A., Lynn, S. G., Goulden, C. E. & Herrera, L. COMBO – A defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377, 147–159 (1998).CAS 
    Article 

    Google Scholar 
    59.Guillard, R. R. L. & Lorenzen, C. J. Yellow-green algae with chlorophyllide c. J. Phycol. 8, 10–14 (1972).CAS 

    Google Scholar 
    60.Balseiro, E. G., Souza, M. S., Modenutti, B. E. & Reissig, M. Living in transparent lakes: Low food P: C ratio decreases antioxidant response to ultraviolet radiation in Daphnia. Limnol. Oceanogr. 53, 2383–2390 (2008).ADS 
    CAS 
    Article 

    Google Scholar 
    61.Laspoumaderes, C., Souza, M. S., Modenutti, B. E. & Balseiro, E. Glacier melting and response of Daphnia oxidative stress. J. Plankton Res. 39, 675–686. https://doi.org/10.1093/plankt/fbx028 (2017).CAS 
    Article 

    Google Scholar 
    62.APHA. Standard methods for the examination of water and wastewater. (American Public Health Association, AWWA, 2005).63.Gorokhova, E. & Kyle, M. Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA-DNA content. J. Plankton Res. 24, 511–522 (2002).CAS 
    Article 

    Google Scholar  More

  • in

    Sex, age, and parental harmonic convergence behavior affect the immune performance of Aedes aegypti offspring

    1.Centers for Disease Control and Prevention https://www.cdc.gov/dengue/areaswithrisk/index.html (2021).2.Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504–507 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Brady, O. J. et al. Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLoS Negl. Trop. Dis. 6, e1760 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Centers for Disease Control and Prevention https://www.cdc.gov/parasites/malaria/index.html (2021)5.Gatton, M. L. et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution 67, 1218–1230 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Sokhna, C., Ndiath, M. O. & Rogier, C. The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. Clin. Microbiol. Infect. 19, 902–907 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Hemingway, J., Hawkes, N. J., McCarroll, L. & Ranson, H. The molecular basis of insecticide resistance in mosquitoes. Insect Biochem. Mol. Biol. 34, 653–665 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Alphey, L. et al. Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis. 10, 295–311 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Oliva, C. F., Damiens, D. & Benedict, M. Q. Male reproductive biology of Aedes mosquitoes. Acta Tropica 132, S12–S19 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Benelli, G. Research in mosquito control: current challenges for a brighter future. Parasitol. Res. 114, 2801–2805 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Lees, R. S., Gilles, J. R. L., Hendrichs, J., Vreysen, M. J. B. & Bourtzis, K. Back to the future: the sterile insect technique against mosquito disease vectors. Curr. Opin. Insect Sci. 10, 156–162 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Wilke, A. B. & Marrelli, M. T. Genetic control of mosquitoes: population suppression strategies. Rev. Inst. Med. Trop. Sao Paulo 54, 287–292 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Alphey, L., Nimmo, D., O’Connell, S. & Alphey, N. Insect population suppression using engineered insects. Adv. Exp. Med. Biol. 627, 93–103 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    14.Carvalho, D. O. et al. Suppression of a field population of Aedes aegypti in Brazil by sustained release of transgenic male mosquitoes. PLoS Negl. Trop. Dis. 9, e0003864 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    15.Wilke, A. B. B. & Marrelli, M. T. Paratransgenesis: a promising new strategy for mosquito vector control. Parasit. Vectors 8, 342 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    16.Hegde, S. & Hughes, G. L. Population modification of Anopheles mosquitoes for malaria control: pathways to implementation. Pathog. Glob. Health 111, 401–402 (2017).PubMed 
    Article 

    Google Scholar 
    17.Carballar-Lejarazu, R. & James, A. A. Population modification of Anopheline species to control malaria transmission. Pathog. Glob. Health 111, 424–35. (2017).PubMed 
    Article 

    Google Scholar 
    18.Li, Y. & Liu, X. A sex-structured model with birth pulse and release strategy for the spread of Wolbachia in mosquito population. J. Theor. Biol. 448, 53–65 (2018).PubMed 
    Article 

    Google Scholar 
    19.Farkas, J. Z., Gourley, S. A., Liu, R. & Yakubu, A. A. Modelling Wolbachia infection in a sex-structured mosquito population carrying West Nile virus. J. Math. Biol. 75, 621–47. (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Zhang, X., Tang, S., Liu, Q., Cheke, R. A. & Zhu, H. Models to assess the effects of non-identical sex ratio augmentations of Wolbachia-carrying mosquitoes on the control of dengue disease. Math. Biosci. 299, 58–72 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Almeida, L., Privat, Y., Strugarek, M. & Vauchelet, N. Optimal releases for population replacement strategies, application to Wolbachia. SIAM Journal on Mathematical Analysis, Society for Industrial and Applied Mathematics 51, 3170–3194 (2019).Article 

    Google Scholar 
    22.Clements, A. N. The Biology of Mosquitoes: Sensory Reception and Behaviour (Chapman & Hall, 1999).23.Downes, J. A. The swarming and mating flight of Diptera. Annu. Rev. Entomol. 14, 271–98. (1969).Article 

    Google Scholar 
    24.Yuval, B. Mating systems of blood-feeding flies. Annu Rev. Entomol. 51, 413–440 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Charlwood, J. D. & Jones, M. D. R. Mating in the mosquito, Anopheles gambiae s.l. Physiol. Entomol. 5, 315–20. (1980).Article 

    Google Scholar 
    26.Pitts, R. J., Mozuraitis, R., Gauvin-Bialecki, A. & Lemperiere, G. The roles of kairomones, synomones and pheromones in the chemically-mediated behaviour of male mosquitoes. Acta Tropica 132, S26–S34 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Hartberg, W. K. Observations on the mating behaviour of Aedes aegypti in nature. Bull. World Health Organ. 45, 847–850 (1971).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    28.Sawadogo P. S. et al. Swarming behaviour in natural populations of Anopheles gambiae and An. coluzzii: review of 4 years survey in rural areas of sympatry, Burkina Faso (West Africa). Acta Tropica 132, S42-52 https://doi.org/10.1016/j.actatropica.2013.12.011 (2014).29.South, A. C. F. Progress in Mosquito Research (Elsevier Science, 2016).30.Cator, L. J. & Harrington, L. C. The harmonic convergence of fathers predicts the mating success of sons in Aedes aegypti. Anim. Behav. 82, 627–633 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Benelli, G. The best time to have sex: mating behaviour and effect of daylight time on male sexual competitiveness in the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae). Parasitol. Res. 114, 887–94. (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    32.Benelli, G., Romano, D., Messing, R. H. & Canale, A. First report of behavioural lateralisation in mosquitoes: right-biased kicking behaviour against males in females of the Asian tiger mosquito, Aedes albopictus. Parasitol. Res. 114, 1613–1617 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Cator, L. J. & Zanti, Z. Size, sounds and sex: interactions between body size and harmonic convergence signals determine mating success in Aedes aegypti. Parasites Vectors 9, 622 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.South, S. H., Steiner, D. & Arnqvist, G. Male mating costs in a polygynous mosquito with ornaments expressed in both sexes. Proc. R. Soc. B 276, 3671–3678 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    35.Roth, L. M. A study of mosquito behavior. An experimental laboratory study of the sexual behavior of Aedes aegypti (Linnaeus). Am. Midl. Nat. 40, 265–352 (1948).Article 

    Google Scholar 
    36.Wishart, G., van Sickle, G. R. & Riordan, D. F. Orientation of the males of Aedes aegypti (L.) (Diptera: Culicidae) to sound. Can. Entomol. 94, 613–26. (1962).Article 

    Google Scholar 
    37.Belton, P. Attraction of male mosquitoes to sound. J. Am. Mosq. Control Assoc. 10, 297–301 (1994).CAS 
    PubMed 

    Google Scholar 
    38.Simões, P. M. V., Ingham, R. A., Gibson, G. & Russell, I. J. A role for acoustic distortion in novel rapid frequency modulation behaviour in free-flying male mosquitoes. J. Exp. Biol. 219, 2039–2047 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    39.Simoes, P. M., Gibson, G. & Russell, I. J. Pre-copula acoustic behaviour of males in the malarial mosquitoes Anopheles coluzzii and Anopheles gambiae s.s. does not contribute to reproductive isolation. J. Exp. Biol. 220, 379–85. (2017).PubMed 
    Article 

    Google Scholar 
    40.Gibson, G. & Russell, I. Flying in tune: sexual recognition in mosquitoes. Curr. Biol. 16, 1311–1316 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Cator, L. J., Arthur, B. J., Harrington, L. C. & Hoy, R. R. Harmonic convergence in the love songs of the dengue vector mosquito. Science 323, 1077–1079 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Warren, B., Gibson, G. & Russell, I. J. Sex recognition through midflight mating duets in culex mosquitoes is mediated by acoustic distortion. Curr. Biol. 19, 485–491 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.Pennetier, C., Warren, B., Dabiré, K. R., Russell, I. J. & Gibson, G. “Singing on the Wing” as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Curr. Biol. 20, 131–136 (2010).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Aldersley, A. & Cator, L. J. Female resistance and harmonic convergence influence male mating success in Aedes aegypti. Sci. Rep. 9, 2145 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    45.League, G. P., Baxter, L. L., Wolfner, M. F. & Harrington, L. C. Male accessory gland molecules inhibit harmonic convergence in the mosquito Aedes aegypti. Curr. Biol. 29, R196–r7. (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Villarreal, S. M. et al. Male contributions during mating increase female survival in the disease vector mosquito Aedes aegypti. J. Insect Physiol. 108, 1–9 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Dobson, A. P. & Hudson, P. J. Regulation and stability of a free-living host–parasite system: Trichostrongylus tenuis in Red Grouse. II. Population models. J. Anim. Ecol. 61, 487–498 (1992).Article 

    Google Scholar 
    48.Hamilton, W. D. & Zuk, M. Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387 (1982).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Hillyer, J. F., Schmidt, S. L. & Christensen, B. M. Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell Tissue Res. 313, 117–127 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Moreno-García, M., Córdoba-Aguilar, A., Condé, R. & Lanz-Mendoza, H. Current immunity markers in insect ecological immunology: assumed trade-offs and methodological issues. Bull. Entomol. Res. 103, 127–139 (2012).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    51.Schoenle, L. A., Downs, C. J. & Martin L. B. An introduction to ecoimmunology. In Advances in Comparative Immunology (ed. Cooper, E. L.). 901–932 (Springer International Publishing, 2018).52.Barthel, A., Staudacher, H., Schmaltz, A., Heckel, D. G. & Groot, A. T. Sex-specific consequences of an induced immune response on reproduction in a moth. BMC Evol. Biol. 15, 282 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    53.Hillyer, J. F. & Strand, M. R. Mosquito hemocyte-mediated immune responses. Curr. Opin. Insect Sci. 3, 14–21 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Chun, J., Riehle, M. & Paskewitz, S. M. Effect of mosquito age and reproductive status on melanization of sephadex beads in Plasmodium-refractory and -susceptible strains of Anopheles gambiae. J. Invertebr. Pathol. 66, 11–17 (1995).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Li, J., Tracy, J. W. & Christensen, B. M. Relationship of hemolymph phenol oxidase and mosquito age in Aedes aegypti. J. Invertebr. Pathol. 60, 188–191 (1992).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Rolff, J. & Siva-Jothy, M. T. Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proc. Natl Acad. Sci. USA 99, 9916–9918 (2002).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Schwenke, R. A. & Lazzaro, B. P. Juvenile hormone suppresses resistance to infection in mated female Drosophila melanogaster. Curr. Biol. 27, 596–601 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Reavey, C. E., Warnock, N. D., Cotter, S. C. & Vogel, H. Trade-offs between personal immunity and reproduction in the burying beetle, Nicrophorus vespilloides. Behav. Ecol. 25, 415–23. (2014).Article 

    Google Scholar 
    59.Christensen, B. M., Li, J. Y., Chen, C. C. & Nappi, A. J. Melanization immune responses in mosquito vectors. Trends Parasitol. 21, 192–199 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Harris, K. L., Christensen, B. M. & Miranpuri, G. S. Comparative studies on the melanization response of male and female mosquitoes against microfilariae. Dev. Comp. Immunol. 10, 305–310 (1986).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    61.Syed, Z. A., Gupta, V., Arun, M. G., Dhiman, A., Nandy, B. & Prasad, N. G. Absence of reproduction-immunity trade-off in male Drosophila melanogaster evolving under differential sexual selection. BMC Evol. Biol. 20, 13 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Schwenke R. A., Lazzaro B. P., Wolfner M. F. Reproduction-immunity trade-offs in insects. Annu. Rev. Entomol. 61, 239–256 (2016).63.Schmid-Hempel, P. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50, 529–551 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Armitage, S. A., Thompson, J. J., Rolff, J. & Siva-Jothy, M. T. Examining costs of induced and constitutive immune investment in Tenebrio molitor. J. Evol. Biol. 16, 1038–1044 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    65.Schwartz, A. & Koella, J. C. The cost of immunity in the yellow fever mosquito, Aedes aegypti depends on immune activation. J. Evol. Biol. 17, 834–840 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Rauw, W. M. Immune response from a resource allocation perspective. Front. Genet. 3, 267 (2012).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    67.Levashina, E. A., Moita, L. F., Blandin, S., Vriend, G., Lagueux, M. & Kafatos, F. C. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104, 709–718 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Strand, M. R. The insect cellular immune response. Insect Sci. 15, 1–14 (2008).CAS 
    Article 

    Google Scholar 
    69.Das, S., Dong, Y., Garver, L. & Dimopoulos, G. Specificity of the Innate Immune System: a Closer Look at the Mosquito Pattern-recognition Receptor Repertoire. (Oxford University Press, 2009).
    Google Scholar 
    70.King, J. G. & Hillyer, J. F. Infection-induced interaction between the mosquito circulatory and immune systems. PLoS Pathog. 8, e1003058–e1003058 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Murdock, C. C., Paaijmans, K. P., Bell, A. S., King, J. G., Hillyer, J. F. & Read, A. F. et al. Complex effects of temperature on mosquito immune function. Proc. R. Soc. B 279, 3357–3366 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    72.Liu, W.-T., Tu, W.-C., Lin, C.-H., Yang, U.-C. & Chen, C.-C. Involvement of cecropin B in the formation of the Aedes aegypti mosquito cuticle. Sci. Rep. 7, 16395 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    73.Hillyer, J. F., Schmidt, S. L., Fuchs, J. F., Boyle, J. P. & Christensen, B. M. Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell. Microbiol. 7, 39–51 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Coggins, S., Estévez-Lao, T. & Hillyer, J. Increased survivorship following bacterial infection by the mosquito Aedes aegypti as compared to Anopheles gambiae correlates with increased transcriptional induction of antimicrobial peptides. Dev. Comp. Immunol. 37, 390–401 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Luckhart, S., Vodovotz, Y., Cui, L. & Rosenberg, R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc. Natl Acad. Sci. USA 95, 5700–5705 (1998).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Graça-Souza, A. V., Maya-Monteiro, C., Paiva-Silva, G. O., Braz, G. R., Paes, M. C. & Sorgine, M. H. et al. Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem. Mol. Biol. 36, 322–335 (2006).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    77.Cirimotich, C. M., Ramirez, J. L. & Dimopoulos G. Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10, 307–310 (2011).78.Sánchez-Vargas, I., Scott, J. C., Poole-Smith, B. K., Franz, A. W., Barbosa-Solomieu, V. & Wilusz, J. et al. Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito’s RNA interference pathway. PLoS Pathog. 5, e1000299 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    79.Souza-Neto, J. A., Sim, S. & Dimopoulos, G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc. Natl Acad. Sci. 106, 17841–17846 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    80.Castillo, J., Brown, M. R. & Strand, M. R. Blood feeding and insulin-like peptide 3 stimulate proliferation of hemocytes in the mosquito Aedes aegypti. PLoS Pathog. 7, e1002274 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.Bryant, W. B. & Michel, K. Blood feeding induces hemocyte proliferation and activation in the African malaria mosquito, Anopheles gambiae Giles. J. Exp. Biol. 217, 1238–1245 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    82.Xi, Z., Ramirez, J. L. & Dimopoulos, G. The Aedes aegypti Toll pathway controls dengue virus infection. PLoS Pathog. 4, e1000098 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    83.Bottino-Rojas, V., Talyuli, O. A., Jupatanakul, N., Sim, S., Dimopoulos, G. & Venancio, T. M. et al. Heme signaling impacts global gene expression, immunity and dengue virus infectivity in Aedes aegypti. PLoS ONE 10, e0135985 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    84.Oliveira, J. H. M., Talyuli, O. A. C., Goncalves, R. L. S., Paiva-Silva, G. O., Sorgine, M. H. F. & Alvarenga, P. H. et al. Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika. PLoS Negl. Trop. Dis. 11, e0005525 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    85.Bernstein, E., Caudy, A. A., Hammond, S. M. & Hannon, G. J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    86.Elbashir, S. M., Lendeckel, W. & Tuschl, T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 15, 188–200 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    87.Miyoshi, K., Tsukumo, H., Nagami, T., Siomi, H. & Siomi, M. C. Slicer function of Drosophila Argonautes and its involvement in RISC formation. Genes Dev. 19, 2837–2848 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    88.Okamura, K., Ishizuka, A., Siomi, H. & Siomi, M. C. Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 18, 1655–1666 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    89.Rand, T. A., Ginalski, K., Grishin, N. V. & Wang, X. Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity. Proc. Natl Acad. Sci. USA 101, 14385–14389 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    90.Ramos-Castaneda, J., Gonzalez, C., Jimenez, M. A., Duran, J., Hernandez-Martinez, S. & Rodriguez, M. H. et al. Effect of nitric oxide on dengue virus replication in Aedes aegypti and Anopheles albimanus. Intervirology 51, 335–341 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    91.Xiao, X., Liu, Y., Zhang, X., Wang, J., Li, Z. & Pang, X. et al. Complement-related proteins control the flavivirus infection of Aedes aegypti by inducing antimicrobial peptides. PLoS Pathog. 10, e1004027 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    92.Waldock, J., Olson, K. E. & Christophides, G. K. Anopheles gambiae antiviral immune response to systemic O’nyong-nyong infection. PLoS Negl. Trop. Dis. 6, e1565 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    93.Colpitts, T. M., Cox, J., Vanlandingham, D. L., Feitosa, F. M., Cheng, G. & Kurscheid, S. et al. Alterations in the Aedes aegypti transcriptome during infection with West Nile, dengue and yellow fever Viruses. PLoS Pathog. 7, e1002189 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    94.Moon, A. E., Walker A. J. & Goodbourn S. Regulation of transcription of the Aedes albopictus cecropin A1 gene: a role for p38 mitogen-activated protein kinase. Insect Biochem. Mol. Biol. 41, 628–636 (2011).95.Jordan, T. X. & Randall, G. Dengue virus activates the AMP kinase-mTOR axis to stimulate a proviral lipophagy. J. Virol. 91, e02020–16 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    96.Urbanowski, M. D. & Hobman, T. C. The West Nile virus capsid protein blocks apoptosis through a phosphatidylinositol 3-kinase-dependent mechanism. J. Virol. 87, 872–881 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Lazzaro, B. P., Flores, H. A., Lorigan, J. G. & Yourth, C. P. Genotype-by-environment interactions and adaptation to local temperature affect immunity and fecundity in Drosophila melanogaster. PLoS Pathog. 4, e1000025 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    98.Jupatanakul, N. et al. Engineered Aedes aegypti JAK/STAT pathway-mediated immunity to dengue virus. PLoS Negl. Trop. Dis. 11, e0005187 (2017).99.Martin-Acebes M. A. et al. The composition of West Nile virus lipid envelope unveils a role of sphingolipid metabolism in flavivirus biogenesis. J. Virol. 88, 12041–12054 (2014).100.Barletta, A. B., Alves, L. R., Silva, M. C., Sim, S., Dimopoulos, G. & Liechocki, S. et al. Emerging role of lipid droplets in Aedes aegypti immune response against bacteria and dengue virus. Sci. Rep. 6, 19928 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    101.Fu, Q., Inankur, B., Yin, J., Striker, R. & Lan, Q. Sterol carrier protein 2, a critical host factor for dengue virus infection, alters the cholesterol distribution in mosquito Aag2 Cells. J. Med. Entomol. 52, 1124–1134 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    102.Jupatanakul, N., Sim, S. & Dimopoulos, G. Aedes aegypti ML and Niemann-Pick type C family members are agonists of dengue virus infection. Dev. Comp. Immunol. 43, 1–9 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    103.Evans, M. V. et al. Carry-over effects of urban larval environments on the transmission potential of dengue-2 virus. Parasites Vectors 11, 426 (2018).104.Salazar, M. I., Richardson, J. H., Sánchez-Vargas, I., Olson, K. E. & Beaty, B. J. Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol. 7, 9 (2007).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    105.Gloria-Soria, A., Soghigian, J., Kellner, D. & Powell, J. R. Genetic diversity of laboratory strains and implications for research: the case of Aedes aegypti. PLoS Negl. Trop. Dis. 13, e0007930 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    106.Souza-Neto, J. A., Powell, J. R. & Bonizzoni, M. Aedes aegypti vector competence studies: a review. Infect. Genet. Evol. 67, 191–209 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    107.Franz, A. W. et al. Fitness impact and stability of a transgene conferring resistance to dengue-2 virus following introgression into a genetically diverse Aedes aegypti strain. PLoS Negl. Trop. Dis. 8, e2833 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    108.Irvin, N., Hoddle, M. S., O’Brochta, D. A., Carey, B. & Atkinson, P. W. Assessing fitness costs for transgenic Aedes aegypti expressing the GFP marker and transposase genes. Proc. Natl Acad. Sci. USA 101, 891–896 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    109.Pompon, J. & Levashina, E. A. A new role of the mosquito complement-like cascade in male fertility in Anopheles gambiae. PLoS Biol. 13, e1002255–e1002255 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    110.Mitchell, S. N., Kakani, E. G., South, A., Howell, P. I., Waterhouse, R. M. & Catteruccia, F. Mosquito biology. Evolution of sexual traits influencing vectorial capacity in anopheline mosquitoes. Science 347, 985–988 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    111.League G. P. et al. Sexual selection theory meets disease vector control: Testing harmonic convergence as a “good genes” signal in Aedes aegypti mosquitoes. Preprint at bioRxiv https://doi.org/10.1101/2020.10.29.360651 (2020).112.Hillyer, J. F. & Estevez-Lao, T. Y. Nitric oxide is an essential component of the hemocyte-mediated mosquito immune response against bacteria. Dev. Comp. Immunol. 34, 141–149 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    113.Warburg, A., Shtern, A., Cohen, N. & Dahan, N. Laminin and a Plasmodium ookinete surface protein inhibit melanotic encapsulation of Sephadex beads in the hemocoel of mosquitoes. Microbes Infect. 9, 192–199 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    114.Lambrechts, L., Vulule, J. M. & Koella, J. C. Genetic correlation between melanization and antibacterial immune responses in a natural population of the malaria vector Anopheles gambiae. Evolution 58, 2377–2381 (2004).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    115.Lambrechts, L., Morlais, I., Awono-Ambene, P. H., Cohuet, A., Simard, F. & Jacques, J.-C. et al. Effect of infection by Plasmodium falciparum on the melanization immune response of Anopheles gambiae. Am. J. Tropic. Med. Hyg. 76, 475–480 (2007).Article 

    Google Scholar 
    116.Boëte, C., Paul, R. E. L. & Koella, J. C. Direct and indirect immunosuppression by a malaria parasite in its mosquito vector. Proc. R. Soc. Lond. Ser. B 271, 1611–1615 (2004).Article 

    Google Scholar 
    117.Ramakrishnan, M. A. Determination of 50% endpoint titer using a simple formula. World J. Virol. 5, 85–86 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    118.Tesla, B., Demakovsky, L. R., Mordecai, E. A., Ryan, S. J., Bonds, M. H. & Ngonghala, C. N. et al. Temperature drives Zika virus transmission: evidence from empirical and mathematical models. Proc. R. Soc. B 285, 20180795 (2018).PubMed 
    Article 

    Google Scholar 
    119.Franz, A. W., Kantor, A. M., Passarelli, A. L. & Clem, R. J. Tissue barriers to arbovirus infection in mosquitoes. Viruses 7, 3741–3767 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    120.Lanciotti, R. S., Calisher, C. H., Gubler, D. J., Chang, G. J. & Vorndam, A. V. Rapid detection and typing of dengue viruses from clinical-samples by using reverse transcriptase-polymerase chain-reaction. J. Clin. Microbiol 30, 545–551 (1992).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    121.RStudio Team. RStudio: Integrated Development Environment for R (RStudio, Inc., 2016).122.R. Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).123.Brooks, M. E., Kristensen, K., van Benthem, K. J., Magnusson, A., Berg, C. W. & Nielsen, A. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R. J. 9, 378–400 (2017).Article 

    Google Scholar 
    124.Christensen, R. H. B. Ordinal-Regression Models for Ordinal Data. R package version 2015.6-28 (R Foundation for Statistical Computing, 2015).125.Bates, D., Mächler, M., Bolker, B. & Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 48 (2015).Article 

    Google Scholar 
    126.Bolker, B. R Development Core Team. bbmle: Tools for General Maximum Likelihood Estimation. R package version 1.0.20 (CRAN, 2017).127.Hartig, F. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.2.4 ed (CRAN, 2019).128.Lenth, R. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.3.3, ed (CRAN, 2019). More

  • in

    Adapted tolerance to virus infections in four geographically distinct Varroa destructor-resistant honeybee populations

    1.Rosenkranz, P., Aumeier, P. & Ziegelmann, B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96–S119 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Wilfert, L. et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science (80–.) 351, 594–597 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    3.Levin, S., Sela, N. & Chejanovsky, N. Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Sci. Rep. 6, 37710 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Tentcheva, D. et al. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol. 70, 7185–7191 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Martin, S. The role of Varroa and viral pathogens in the collapse of honeybee colonies: A modeling approach. J. Appl. Ecol. 38, 1082–1093 (2001).Article 

    Google Scholar 
    6.Mordecai, G. J., Wilfert, L., Martin, S. J., Jones, I. M. & Schroeder, D. C. Diversity in a honey bee pathogen: First report of a third master variant of the Deformed Wing Virus quasispecies. ISME J. 10, 1264–1273 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.de Miranda, J. R., Cordoni, G. & Budge, G. The Acute bee paralysis virus—Kashmir bee virus—Israeli acute paralysis virus complex. J. Invertebr. Pathol. 103, S30–S47 (2010).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    8.de Miranda, J. R. & Genersch, E. Deformed wing virus. J. Invertebr. Pathol. 103, 48–61 (2010).Article 
    CAS 

    Google Scholar 
    9.Bowen-Walker, P. L., Martin, S. J. & Gunn, A. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J. Invertebr. Pathol. 73, 101–106 (1999).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Yue, C., Schroeder, M., Gisder, S. & Genersch, E. Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J. Gen. Virol. 88, 2329–2336 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.de Miranda, J. R. & Fries, I. Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J. Invertebr. Pathol. 98, 184–189 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Genersch, E. & Aubert, M. Emerging and re-emerging viruses of the honey bee (Apis mellifera L). Vet. Res. 41, 54 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    13.de Miranda, J. R. et al. Standard methods for virus research in Apis mellifera. J. Apic. Res. 52, 1–56 (2013).ADS 
    Article 
    CAS 

    Google Scholar 
    14.Amiri, E. et al. Quantitative patterns of vertical transmission of deformed wing virus in honey bees. PLoS ONE 13, e0195283 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    15.Moeckel, N., Gisder, S. & Genersch, E. Horizontal transmission of deformed wing virus: Pathological consequences in adult bees (Apis mellifera) depend on the transmission route. J. Gen. Virol. 92, 370–377 (2011).CAS 
    Article 

    Google Scholar 
    16.Boecking, O. & Genersch, E. Varroosis—The ongoing crisis in bee keeping. J. für Verbraucherschutz und Leb. 3, 221–228 (2008).Article 

    Google Scholar 
    17.Locke, B. Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 47, 467–482 (2016).Article 

    Google Scholar 
    18.Locke, B. & Fries, I. Characteristics of honey bee colonies (Apis mellifera) in Sweden surviving Varroa destructor infestation. Apidologie 42, 533–542 (2011).Article 

    Google Scholar 
    19.Locke, B., Le Conte, Y., Crauser, D. & Fries, I. Host adaptations reduce the reproductive success of Varroa destructor in two distinct European honey bee populations. Ecol. Evol. 2, 1144–1150 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Oddie, M. A. Y., Dahle, B. & Neumann, P. Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection. PeerJ 5, e3956 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Panziera, D., van Langevelde, F. & Blacquière, T. Varroa sensitive hygiene contributes to naturally selected varroa resistance in honey bees. J. Apic. Res. 56, 635–642 (2017).Article 

    Google Scholar 
    22.Schmid-Hempel, P. Parasites and their social hosts. Trends Parasitol. 33, 453–462 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Thaduri, S., Stephan, J. G., de Miranda, J. R. & Locke, B. Disentangling host–parasite–pathogen interactions in a varroa-resistant honeybee population reveals virus tolerance as an independent, naturally adapted survival mechanism. Sci. Rep. 9, 6221 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    24.Locke, B., Forsgren, E. & de Miranda, J. R. Increased tolerance and resistance to virus infections: A possible factor in the survival of Varroa destructor-resistant honey bees (Apis mellifera). PLoS ONE 9, e99998 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    25.Thaduri, S., Locke, B., Granberg, F. & de Miranda, J. R. Temporal changes in the viromes of Swedish Varroa-resistant and Varroa-susceptible honeybee populations. PLoS ONE 13, e0206938 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Le Conte, Y. et al. Honey bee colonies that have survived Varroa destructor. Apidologie 38, 566–572 (2007).Article 

    Google Scholar 
    27.Fries, I., Imdorf, A. & Rosenkranz, P. Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie 37, 564–570 (2006).Article 

    Google Scholar 
    28.Dietemann, V. et al. Standard methods for varroa research. J. Apic. Res. 52, 1–54 (2013).
    Google Scholar 
    29.Meeus, I., de Miranda, J. R., de Graaf, D. C., Wäckers, F. & Smagghe, G. Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success. J. Invertebr. Pathol. 121, 64–69 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Carrillo-Tripp, J. et al. In vivo and in vitro infection dynamics of honey bee viruses. Sci. Rep. 6, 22265 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Aupinel, P. et al. Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bull. Insectol. 58, 107–111 (2005).
    Google Scholar 
    32.Crailsheim, K. et al. Standard methods for artificial rearing of Apis mellifera larvae. J. Apic. Res. 52, 1–16 (2013).Article 

    Google Scholar 
    33.Forsgren, E., Locke, B., Semberg, E., Laugen, A. T. & de Miranda, J. R. Sample preservation, transport and processing strategies for honeybee RNA extraction: Influence on RNA yield, quality, target quantification and data normalization. J. Virol. Methods 246, 81–89 (2017).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Williams, G. R. et al. Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J. Apic. Res. 52, 1–36 (2013).Article 

    Google Scholar 
    35.Locke, B., Forsgren, E., Fries, I. & de Miranda, J. R. Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control. Appl. Environ. Microbiol. 78, 227–235 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Lourenco, A. P., Mackert, A., Cristino, A. D. S. & Simoes, Z. L. P. Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie 39, 372–385 (2008).CAS 
    Article 

    Google Scholar 
    37.R Core Team. R: A language and environment for statistical computing (2017).38.Kuznetsova, A., Brockhoff, P. & Christensen, R. H. B. Package ‘lmerTest’: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).Article 

    Google Scholar 
    39.Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).Article 

    Google Scholar 
    40.Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biometrical J. 50, 346–363 (2008).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    41.Cox, D. R. Regression models and life-tables. J. R. Stat. Soc. Ser. B 34, 187–202 (1972).MathSciNet 
    MATH 

    Google Scholar 
    42.Therneau, T. M. & Grambsch, P. M. The Cox model 39–77 (Springer, 2000). https://doi.org/10.1007/978-1-4757-3294-8_3.Book 
    MATH 

    Google Scholar 
    43.Schoenfeld, D. Chi-squared goodness-of-fit tests for the proportional hazards regression model. Biometrika 67, 145–153 (1980).MathSciNet 
    MATH 
    Article 

    Google Scholar 
    44.Therneau, T. M. Package ‘coxme’: Mixed effects Cox models. R package version 2.2-10; 2018 (2018).45.De Jong, P. S., De Jong, L. & Goncalves, D. H. Weight loss and other damage to developing worker honeybees from infestation with Varroa Jacobsoni. J. Apic. Res. https://doi.org/10.1080/00218839.1982.11100535 (1983).Article 

    Google Scholar 
    46.Sumpter, D. J. T. & Martin, S. J. The dynamics of virus epidemics in Varroa-infested honey bee colonies. J. Anim. Ecol. 73, 51–63 (2004).Article 

    Google Scholar 
    47.Mondet, F., de Miranda, J. R., Kretzschmar, A., Le Conte, Y. & Mercer, A. R. On the front line: Quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathog. 10, e1004323 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    48.Mondet, F. et al. Specific cues associated with honey bee social defence against Varroa destructor infested brood. Sci. Rep. 6, 25444 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    49.Brutscher, L. M., Daughenbaugh, K. F. & Flenniken, M. L. Antiviral defense mechanisms in honey bees. Curr. Opin. Insect Sci. 10, 71–82 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Martin, S. J. & Brettell, L. E. Deformed wing virus in honeybees and other insects. Annu. Rev. Virol. 6, annurev-virology-092818-015700 (2019).Article 
    CAS 

    Google Scholar 
    51.Grozinger, C. M. & Flenniken, M. L. Bee viruses: Ecology, pathogenicity, and impacts. Annu. Rev. Entomol. 64, 205–226 (2019).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Amiri, E., Meixner, M. D. & Kryger, P. Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Sci. Rep. 6, 33065 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Yue, C. & Genersch, E. RT-PCR analysis of deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J. Gen. Virol. 86, 3419–3424 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    54.Chen, Y., Evans, J. & Feldlaufer, M. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J. Invertebr. Pathol. 92, 152–159 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Gauthier, L. et al. Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLoS ONE 6, e16217 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Nordström, S., Fries, I., Aarhus, A., Hansen, H. & Korpela, S. Virus infections in Nordic honey bee colonies with no, low or severe Varroa jacobsoni infestations. Apidologie 30, 475–484 (1999).Article 

    Google Scholar 
    57.Biesmeijer, K. Report Honeybee Surveillance Program the Netherlands 2006–2017. (2017).58.Strauss, U. et al. Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata). J. Invertebr. Pathol. 114, 45–52 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Khongphinitbunjong, K. et al. Responses of Varroa-resistant honey bees (Apis mellifera L.) to deformed wing virus. J. Asia Pac. Entomol. 19, 921–927 (2016).Article 

    Google Scholar 
    60.Råberg, L., Graham, A. L. & Read, A. F. Decomposing health: Tolerance and resistance to parasites in animals. Philos. Trans. R. Soc. B 364, 37–49 (2009).Article 

    Google Scholar 
    61.Thompson, J. N. The Coevolutionary Process (University of Chicago Press, 1994).Book 

    Google Scholar 
    62.Ongus, J. R. et al. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol. 85, 3747–3755 (2004).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Gisder, S., Aumeier, P. & Genersch, E. Deformed wing virus: Replication and viral load in mites (Varroa destructor). J. Gen. Virol. 90, 463–467 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    64.Nazzi, F. et al. Synergistic parasite–pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog. 8, e1002735 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Yang, X. & Cox-Foster, D. L. Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proc. Natl. Acad. Sci. 102, 7470–7475 (2005).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Yang, X. & Cox-Foster, D. Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 134, 405 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    67.Ryabov, E. V. et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro transmission. PLoS Pathog. 10, e1004230 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    68.Ryabov, E. V., Fannon, J. M., Moore, J. D., Wood, G. R. & Evans, D. J. The Iflaviruses Sacbrood virus and Deformed wing virus evoke different transcriptional responses in the honeybee which may facilitate their horizontal or vertical transmission. PeerJ 4, e1591 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    69.Desai, S. D., Eu, Y.-J., Whyard, S. & Currie, R. W. Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion. Insect Mol. Biol. 21, 446–455 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    70.Maori, E. et al. IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion. Insect Mol. Biol. 18, 55–60 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    71.Di Prisco, G. et al. A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. Proc. Natl. Acad. Sci. 113, 3203–3208 (2016).ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar  More

  • in

    Novel clades of soil biphenyl degraders revealed by integrating isotope probing, multi-omics, and single-cell analyses

    1.Singer E, Wagner M, Woyke T. Capturing the genetic makeup of the active microbiome in situ. ISME J. 2017;11:1949–63.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Hall EK, Bernhardt ES, Bier RL, Bradford MA, Boot CM, Cotner JB, et al. Understanding how microbiomes influence the systems they inhabit. Nat Microbiol. 2018;3:977–82.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    3.Lloyd KG, Steen AD, Ladau J, Yin J, Crosby L. Phylogenetically novel uncultured microbial cells dominate earth microbiomes. mSystems 2018;3:e00055–18.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Lewis WH, Tahon G, Geesink P, Sousa DZ, Ettema TJG. Innovations to culturing the uncultured microbial majority. Nat Rev Microbiol. 2021;19:225–40.CAS 
    Article 

    Google Scholar 
    5.Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, et al. A new view of the tree of life. Nat Microbiol. 2016;1:16048.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Spang A, Caceres EF, Ettema TJG. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science. 2017;357:eaaf3883.7.Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ, Evans PN, et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol. 2017;2:1533–42.CAS 
    Article 

    Google Scholar 
    8.Chen S-C, Musat N, Lechtenfeld OJ, Paschke H, Schmidt M, Said N, et al. Anaerobic oxidation of ethane by archaea from a marine hydrocarbon seep. Nature 2019;568:108–11.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F, et al. A genomic catalog of Earth’s microbiomes. Nat Biotechnol. 2021;39:499–509.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Hatzenpichler R, Krukenberg V, Spietz RL, Jay ZJ. Next-generation physiology approaches to study microbiome function at single cell level. Nat Rev Microbiol. 2020;18:241–56.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Baker BJ, De Anda V, Seitz KW, Dombrowski N, Santoro AE, Lloyd KG. Diversity, ecology and evolution of Archaea. Nat Microbiol. 2020;5:887–900.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    12.Abraham WR, Nogales B, Golyshin PN, Pieper DH, Timmis KN. Polychlorinated biphenyl-degrading microbial communities in soils and sediments. Curr Opin Microbiol. 2002;5:246–53.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Galbán-Malagón C, Berrojalbiz N, Ojeda M-J, Dachs J. The oceanic biological pump modulates the atmospheric transport of persistent organic pollutants to the Arctic. Nat Commun 2012;3:862.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    14.Pieper DH. Aerobic degradation of polychlorinated biphenyls. Appl Microbiol Biotechnol. 2005;67:170–91.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Chain PSG, Denef VJ, Konstantinidis KT, Vergez LM, Agulló L, Reyes VL, et al. Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA. 2006;103:15280.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Furukawa K, Suenaga H, Goto M. Biphenyl dioxygenases: functional versatilities and directed evolution. J Bacteriol. 2004;186:5189–96.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.McLeod MP, Warren RL, Hsiao WWL, Araki N, Myhre M, Fernandes C, et al. The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA. 2006;103:15582.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    18.Lee TK, Lee J, Sul WJ, Iwai S, Chai BC, Tiedje JM, et al. Novel biphenyl-oxidizing bacteria and dioxygenase genes from a Korean tidal mudflat. Appl Environ Microbiol. 2011;77:3888–91.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Sul WJ, Park J, Quensen JF, Rodrigues JLM, Seliger L, Tsoi TV, et al. DNA-stable isotope probing integrated with metagenomics for retrieval of biphenyl dioxygenase genes from polychlorinated biphenyl-contaminated river sediment. Appl Environ Microbiol. 2009;75:5501–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Uhlik O, Jecna K, Mackova M, Vlcek C, Hroudova M, Demnerova K, et al. Biphenyl-metabolizing bacteria in the rhizosphere of horseradish and bulk soil contaminated by polychlorinated biphenyls as revealed by stable isotope probing. Appl Environ Microbiol. 2009;75:6471.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Jiang LF, Luo CL, Zhang DY, Song MK, Sun YT, Zhang G. Biphenyl-Metabolizing microbial community and a functional operon revealed in e-waste-contaminated soil. Environ Sci Technol. 2018;52:8558–67.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Tillmann S, Strompl C, Timmis KN, Abraham WR. Stable isotope probing reveals the dominant role of Burkholderia species in aerobic degradation of PCBs. FEMS Microbiol Ecol. 2005;52:207–17.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Leigh MB, Pellizari VH, Uhlik O, Sutka R, Rodrigues J, Ostrom NE, et al. Biphenyl-utilizing bacteria and their functional genes in a pine root zone contaminated with polychlorinated biphenyls (PCBs). ISME J. 2007;1:134–48.CAS 
    Article 

    Google Scholar 
    24.Chen S-C, Duan G-L, Ding K, Huang F-Y, Zhu Y-G. DNA stable-isotope probing identifies uncultivated members of Pseudonocardia associated with biodegradation of pyrene in agricultural soil. FEMS Microbiol Ecol. 2018;94:fiy026.25.Neufeld JD, Dumont MG, Vohra J, Murrell JC. Methodological considerations for the use of stable isotope probing in microbial ecology. Micro Ecol. 2007;53:435–42.CAS 
    Article 

    Google Scholar 
    26.Neufeld JD, Vohra J, Dumont MG, Lueders T, Manefield M, Friedrich MW, et al. DNA stable-isotope probing. Nat Protoc. 2007;2:860–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Mohn WW, Westerberg K, Cullen WR, Reimer KJ. Aerobic biodegradation of biphenyl and polychlorinated biphenyls by Arctic soil microorganisms. Appl Environ Microbiol. 1997;63:3378–84.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Wagner-Dobler I, Bennasar A, Vancanneyt M, Strompl C, Brummer I, Eichner C, et al. Microcosm enrichment of biphenyl-degrading microbial communities from soils and sediments. Appl Environ Microbiol. 1998;64:3014–22.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Allen MB. Studies with cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol. 1959;32:270–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Rabus R, Widdel F. Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol. 1995;163:96–103.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    31.Zhou J, Bruns MA, Tiedje JM. DNA recovery from soils of diverse composition. Appl Environ Microbiol. 1996;62:316.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013;41:D590–D6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Ouyang WY, Su JQ, Richnow HH, Adrian L. Identification of dominant sulfamethoxazole-degraders in pig farm-impacted soil by DNA and protein stable isotope probing. Environ Int. 2019;126:118–26.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    35.Tischer K, Zeder M, Klug R, Pernthaler J, Schattenhofer M, Harms H, et al. Fluorescence in situ hybridization (CARD-FISH) of microorganisms in hydrocarbon contaminated aquifer sediment samples. Syst Appl Microbiol. 2012;35:526–32.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MMM. Look@NanoSIMS–a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. 2012;14:1009–23.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Stryhanyuk H, Calabrese F, Kümmel S, Musat F, Richnow HH, Musat N. Calculation of single cell assimilation rates from SIP-NanoSIMS-derived isotope ratios: a comprehensive approach. Front Microbiol. 2018;9:2342.38.Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Kang DD, Li F, Kirton E, Thomas A, Egan R, An H, et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 2019;7:e7359–e.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 2020;36:1925–7.CAS 

    Google Scholar 
    43.Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–3.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma. 2010;11:119.Article 
    CAS 

    Google Scholar 
    45.Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42:D222–D30.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    47.Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 2019;47:D309–D14. (D1)CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    48.Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinforma. 2009;10:421.Article 
    CAS 

    Google Scholar 
    49.Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    51.Budhraja R, Karande S, Ding C, Ullrich MK, Wagner S, Reemtsma T, et al. Characterization of membrane-bound metalloproteins in the anaerobic ammonium-oxidizing bacterium “Candidatus Kuenenia stuttgartiensis” strain CSTR1. Talanta. 2021;223:121711.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Craig R, Beavis RC. TANDEM: matching proteins with tandem mass spectra. Bioinformatics. 2004;20:1466–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    53.Röst HL, Sachsenberg T, Aiche S, Bielow C, Weisser H, Aicheler F, et al. OpenMS: a flexible open-source software platform for mass spectrometry data analysis. Nat Methods. 2016;13:741–8.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    54.Sachsenberg T, Herbst F-A, Taubert M, Kermer R, Jehmlich N, von Bergen M, et al. MetaProSIP: automated inference of stable isotope incorporation rates in proteins for functional metaproteomics. J Proteome Res. 2015;14:619–27.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    55.Liu J, He XX, Lin XR, Chen WC, Zhou QX, Shu WS, et al. Ecological effects of combined pollution associated with e-waste recycling on the composition and diversity of soil microbial communities. Environ Sci Technol. 2015;49:6438–47.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    56.Kumamaru T, Suenaga H, Mitsuoka M, Watanabe T, Furukawa K. Enhanced degradation of polychlorinated biphenyls by directed evolution of biphenyl dioxygenase. Nat Biotechnol. 1998;16:663–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    57.Garrido-Sanz D, Manzano J, Martín M, Redondo-Nieto M, Rivilla R. Metagenomic analysis of a biphenyl-degrading soil bacterial consortium reveals the metabolic roles of specific populations. Front Microbiol. 2018;9:232.58.Kikuchi Y, Nagata Y, Ohtsubo Y, Koana T, Takagi M. Pseudomonas fluorescens KKL101, a benzoic acid degrader in a mixed culture that degrades biphenyl and polychlorinated biphenyls. Biosci Biotechnol Biochem. 1995;59:2303–4.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Musat N, Halm H, Winterholler B, Hoppe P, Peduzzi S, Hillion F, et al. A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc Natl Acad Sci USA. 2008;105:17861.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    60.Calabrese F, Voloshynovska I, Musat F, Thullner M, Schlömann M, Richnow HH, et al. Quantitation and comparison of phenotypic heterogeneity among single cells of monoclonal microbial populations. Front Microbiol. 2019;10:2814.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Robertson BR, Button DK, Koch AL. Determination of the biomasses of small bacteria at low concentrations in a mixture of species with forward light scatter measurements by flow cytometry. Appl Environ Microbiol. 1998;64:3900–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    62.Troussellier M, Bouvy M, Courties C, Dupuy C. Variation of carbon content among bacterial species under starvation condition. Aquat Micro Ecol. 1997;13:113–9.Article 

    Google Scholar 
    63.Furukawa K, Miyazaki T. Cloning of a gene cluster encoding biphenyl and chlorobiphenyl degradation in Pseudomonas pseudoalcaligenes. J Bacteriol. 1986;166:392–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Seeger M, Timmis KN, Hofer B. Conversion of chlorobiphenyls into phenylhexadienoates and benzoates by the enzymes of the upper pathway for polychlorobiphenyl degradation encoded by the bph locus of Pseudomonas sp. strain LB400. Appl Environ Microbiol. 1995;61:2654–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Chadhain SM, Moritz EM, Kim E, Zylstra GJ. Identification, cloning, and characterization of a multicomponent biphenyl dioxygenase from Sphingobium yanoikuyae B1. J Ind Microbiol Biotechnol. 2007;34:605–13.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Hofer B, Backhaus S, Timmis KN. The biphenyl/polychlorinated biphenyl-degradation locus (bph) of Pseudomonas sp. LB400 encodes four additional metabolic enzymes. Gene 1994;144:9–16.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    67.Harwood CS, Parales RE. The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol. 1996;50:553–90.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    68.Rather LJ, Knapp B, Haehnel W, Fuchs G. Coenzyme A-dependent aerobic metabolism of benzoate via epoxide formation. J Biol Chem. 2010;285:20615–24.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    69.Stegen JC, Fredrickson JK, Wilkins MJ, Konopka AE, Nelson WC, Arntzen EV, et al. Groundwater-surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover. Nat Commun. 2016;7:1–12.70.Corteselli EM, Aitken MD, Singleton DR. Rugosibacter aromaticivorans gen. nov., sp. nov., a bacterium within the family Rhodocyclaceae, isolated from contaminated soil, capable of degrading aromatic compounds. Int J Syst Evol Microbiol 2017;67:311–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Fernandez H, Prandoni N, Fernandez-Pascual M, Fajardo S, Morcillo C, Diaz E, et al. Azoarcus sp. CIB, an anaerobic biodegrader of aromatic compounds shows an endophytic lifestyle. PLoS ONE. 2014;9:e110771.72.Iwai S, Johnson TA, Chai BL, Hashsham SA, Tiedje JM. Comparison of the specificities and efficacies of primers for aromatic dioxygenase gene analysis of environmental samples. Appl Environ Microbiol. 2011;77:3551–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Top EM, Springael D. The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol. 2003;14:262–9.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Dombrowski N, Donaho JA, Gutierrez T, Seitz KW, Teske AP, Baker BJ. Reconstructing metabolic pathways of hydrocarbon-degrading bacteria from the Deepwater Horizon oil spill. Nat Microbiol. 2016;1:1–7.75.de Lorenzo V. Systems biology approaches to bioremediation. Curr Opin Biotechnol. 2008;19:579–89.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    76.Rabus R, Wöhlbrand L, Thies D, Meyer M, Reinhold-Hurek B, Kämpfer P. Aromatoleum gen. nov., a novel genus accommodating the phylogenetic lineage including Azoarcus evansii and related species, and proposal of Aromatoleum aromaticum sp. nov., Aromatoleum petrolei sp. nov., Aromatoleum bremense sp. nov., Aromatoleum toluolicum sp. nov. and Aromatoleum diolicum sp. nov. Int J Syst Evol Microbiol. 2019;69:982–97.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    77.Vogt C, Richnow HH. Bioremediation via in situ microbial degradation of organic pollutants. Adv Biochem Engin/Biotechnol. 2014;142:123–46.
    Google Scholar 
    78.Cunningham JA, Rahme H, Hopkins GD, Lebron C, Reinhard M. Enhanced in situ bioremediation of BTEX-contaminated groundwater by combined injection of nitrate and sulfate. Environ Sci Technol. 2001;35:1663–70.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    79.Mondello FJ, Turcich MP, Lobos JH, Erickson BD. Identification and modification of biphenyl dioxygenase sequences that determine the specificity of polychlorinated biphenyl degradation. Appl Environ Microbiol. 1997;63:3096–103.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    80.Gomez-Gil L, Kumar P, Barriault D, Bolin JT, Sylvestre M, Eltis LD. Characterization of biphenyl dioxygenase of Pandoraea pnomenusa B-356 as a potent polychlorinated biphenyl-degrading enzyme. J Bacteriol. 2007;189:5705–15.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Experimental warming differentially affects vegetative and reproductive phenology of tundra plants

    1.Pepin, N. et al. Elevation-dependent warming in mountain regions of the world. Nat. Clim. Chang. 5, 424–430 (2015).ADS 

    Google Scholar 
    2.Cohen, J. et al. Recent Arctic amplification and extreme mid-latitude weather. Nat. Geosci. 7, 627–637 (2014).ADS 
    CAS 

    Google Scholar 
    3.Overland, J. E., Wang, M., Walsh, J. E. & Stroeve, J. C. Future Arctic climate changes: adaptation and mitigation time scales. Earth’s Future 2, 68–74 (2014).ADS 

    Google Scholar 
    4.Oberbauer, S. F. et al. Phenological response of tundra plants to background climate variation tested using the International Tundra Experiment. Philos. Trans. R. Soc. B Biol. Sci. 368, 1624 (2013).5.Prevéy, J. S. et al. Warming shortens flowering seasons of tundra plant communities. Nat. Ecol. Evol. 3, 45–52 (2019).PubMed 

    Google Scholar 
    6.Jabis, M. D., Winkler, D. E. & Kueppers, L. M. Warming acts through earlier snowmelt to advance but not extend alpine community flowering. Ecology https://doi.org/10.1002/ecy.3108 (2020).7.Beard, K. H., Kelsey, K. C., Leffler, A. J. & Welker, J. M. The missing angle: ecosystem consequences of phenological mismatch. Trends Ecol. Evol. 34, 885–888 (2019).PubMed 

    Google Scholar 
    8.Gallinat, A. S., Primack, R. B. & Wagner, D. L. Autumn, the neglected season in climate change research. Trends Ecol. Evol. 30, 169–176 (2015).PubMed 

    Google Scholar 
    9.Semenchuk, P. R. et al. High Arctic plant phenology is determined by snowmelt patterns but duration of phenological periods is fixed: an example of periodicity. Environ. Res. Lett. 11, 125006 (2016).10.Keenan, T. F. & Richardson, A. D. The timing of autumn senescence is affected by the timing of spring phenology: Implications for predictive models. Glob. Chang. Biol. 21, 2634–2641 (2015).ADS 
    PubMed 

    Google Scholar 
    11.Diepstraten, R. A. E., Jessen, T. D., Fauvelle, C. M. D. & Musiani, M. M. Does climate change and plant phenology research neglect the Arctic tundra? Ecosphere 9, e02362 (2018).12.Savage, J. A. A temporal shift in resource allocation facilitates flowering before leaf out and spring vessel maturation in precocious species. Am. J. Bot. 106, 113–122 (2019).PubMed 

    Google Scholar 
    13.Neuner, G. Frost resistance in alpine woody plants. Front. Plant Sci. 5, 654 (2014).14.Kuprian, E., Briceño, V. F., Wagner, J. & Neuner, G. Ice barriers promote supercooling and prevent frost injury in reproductive buds, flowers and fruits of alpine dwarf shrubs throughout the summer. Environ. Exp. Bot. 106, 4–12 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    15.Vitasse, Y., Lenz, A. & Körner, C. The interaction between freezing tolerance and phenology in temperate deciduous trees. Front. Plant Sci. 5, 1–12 (2014).
    Google Scholar 
    16.Maron, J. L., Agrawal, A. A. & Schemske, D. W. Plant–herbivore coevolution and plant speciation. Ecology 100, 1–11 (2019).
    Google Scholar 
    17.Rafferty, N. E. & Ives, A. R. Effects of experimental shifts in flowering phenology on plant-pollinator interactions. Ecol. Lett. 14, 69–74 (2011).PubMed 

    Google Scholar 
    18.Fitter, A. H. & Fitter, R. S. R. Rapid changes in flowering time in British plants. Science 296, 1689–1691 (2002).ADS 
    CAS 
    PubMed 

    Google Scholar 
    19.Post, E. Time in Ecology: A Theoretical Framework (Princeton University Press, 2019).20.Kharouba, H. M., Vellend, M., Sarfraz, R. M. & Myers, J. H. The effects of experimental warming on the timing of a plant-insect herbivore interaction. J. Anim. Ecol. 84, 785–796 (2015).PubMed 

    Google Scholar 
    21.Zohner, C. M., Mo, L. & Renner, S. S. Global warming reduces leaf-out and flowering synchrony among individuals. Elife 7, 1–15 (2018).
    Google Scholar 
    22.Wipf, S., Stoeckli, V. & Bebi, P. Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Clim. Change 94, 105–121 (2009).ADS 

    Google Scholar 
    23.Bjorkman, A. D., Elmendorf, S. C., Beamish, A. L., Vellend, M. & Henry, G. H. R. Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades. Glob. Chang. Biol. 21, 4651–4661 (2015).ADS 
    PubMed 

    Google Scholar 
    24.Assmann, J. J. et al. Local snow melt and temperature—but not regional sea ice—explain variation in spring phenology in coastal Arctic tundra. Glob. Chang. Biol. 25, 2258–2274 (2019).ADS 
    PubMed 

    Google Scholar 
    25.Cooper, E. J., Dullinger, S. & Semenchuk, P. Late snowmelt delays plant development and results in lower reproductive success in the High Arctic. Plant Sci. 180, 157–167 (2011).CAS 
    PubMed 

    Google Scholar 
    26.Kelsey, K. C. et al. Winter snow and spring temperature have differential effects on vegetation phenology and productivity across Arctic plant communities. Glob. Chang. Biol. 1–15 https://doi.org/10.1111/gcb.15505 (2020).27.Menzel, A. et al. European phenological response to climate change matches the warming pattern. Glob. Chang. Biol. 12, 1969–1976 (2006).ADS 

    Google Scholar 
    28.Panchen, Z. A. & Gorelick, R. Prediction of Arctic plant phenological sensitivity to climate change from historical records. Ecol. Evol. 7, 1325–1338 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    29.Livensperger, C. et al. Earlier snowmelt and warming lead to earlier but not necessarily more plant growth. AoB Plants 8, 1–15 (2016).
    Google Scholar 
    30.Livensperger, C. et al. Experimentally warmer and drier conditions in an Arctic plant community reveal microclimatic controls on senescence. Ecosphere 10, e02677 (2019).31.Piao, S. et al. Plant phenology and global climate change: current progresses and challenges. Glob. Chang. Biol. 1922–1940 https://doi.org/10.1111/gcb.14619 (2019).32.Panchen, Z. A. et al. Substantial variation in leaf senescence times among 1360 temperate woody plant species: implications for phenology and ecosystem processes. Ann. Bot. 865–873 https://doi.org/10.1093/aob/mcv015 (2015).33.Wu, C. et al. Contrasting responses of autumn-leaf senescence to daytime and night-time warming. Nat. Clim. Chang. 8, 1092–1096 (2018).ADS 
    CAS 

    Google Scholar 
    34.Zhu, W. et al. Extension of the growing season due to delayed autumn over mid and high latitudes in North America during 1982–2006. Glob. Ecol. Biogeogr. 21, 260–271 (2012).
    Google Scholar 
    35.Liu, Q. et al. Delayed autumn phenology in the Northern Hemisphere is related to change in both climate and spring phenology. Glob. Chang. Biol. 22, 3702–3711 (2016).ADS 
    PubMed 

    Google Scholar 
    36.Richardson, A. D. et al. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric. Meteorol. 169, 156–173 (2013).
    Google Scholar 
    37.Marchand, F. L. et al. Climate warming postpones senescence in High Arctic Tundra. Arct. Antarct. Alp. Res. 36, 390–394 (2004).
    Google Scholar 
    38.Steltzer, H. & Post, E. Seasons and life cycles. Science 324, 886–887 (2009).PubMed 

    Google Scholar 
    39.Jiang, L. L. et al. Relatively stable response of fruiting stage to warming and cooling relative to other phenological events. Ecology 97, 1961–1969 (2016).CAS 
    PubMed 

    Google Scholar 
    40.Kharouba, H. M. et al. Global shifts in the phenological synchrony of species interactions over recent decades. Proc. Natl Acad. Sci. USA 115, 5211–5216 (2018).CAS 
    PubMed 

    Google Scholar 
    41.Piao, S., Friedlingstein, P., Ciais, P., Viovy, N. & Demarty, J. Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Glob. Biogeochem. Cycles 21, 1–11 (2007).
    Google Scholar 
    42.Wookey, P. A. et al. Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Glob. Chang. Biol. 15, 1153–1172 (2009).ADS 

    Google Scholar 
    43.Arft, A. M. et al. Responses of Tundra plants to experimental warming: meta-analysis of the International Tundra Experiment. Ecol. Monogr. 69, 491–511 (1999).
    Google Scholar 
    44.Buttler, A. et al. Experimental warming interacts with soil moisture to discriminate plant responses in an ombrotrophic peatland. J. Veg. Sci. 26, 964–974 (2015).
    Google Scholar 
    45.Healy, N. C., Oberbauer, S. F. & Hollister, R. D. Examination of surface temperature modification by open-top chambers along moisture and latitudinal gradients in Arctic Alaska using thermal infrared photography. Remote Sens. 1–19 https://doi.org/10.3390/rs8010054 (2016).46.Elmendorf, S. C. et al. Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol. Lett. 15, 164–175 (2012).PubMed 

    Google Scholar 
    47.Post, E., Steinman, B. A. & Mann, M. E. Acceleration of phenological advance and warming with latitude over the past century. Sci. Rep. 1–8 https://doi.org/10.1038/s41598-018-22258-0 (2018).48.Iler, A. M., Høye, T. T., Inouye, D. W. & Schmidt, N. M. Nonlinear flowering responses to climate: Are species approaching their limits of phenological change? Philos. Trans. R. Soc. B Biol. Sci. 368, 13–16 (2013).
    Google Scholar 
    49.Prevéy, J. et al. Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes. Glob. Chang. Biol. 23, 2660–2671 (2017).ADS 
    PubMed 

    Google Scholar 
    50.Wipf, S. & Rixen, C. A review of snow manipulation experiments in Arctic and Alpine Tundra ecosystems. Polar Res. 29, 95–109 (2010).
    Google Scholar 
    51.Bokhorst, S. et al. Variable temperature effects of open top chambers at polar and alpine sites explained by irradiance and snow depth. Glob. Chang. Biol. 19, 64–74 (2013).ADS 
    PubMed 

    Google Scholar 
    52.Zhu, J., Zhang, Y. & Wang, W. Interactions between warming and soil moisture increase overlap in reproductive phenology among species in an alpine meadow. Biol. Lett. 12, 1–4 (2016).ADS 

    Google Scholar 
    53.Kemppinen, J., Niittynen, P., Aalto, J., le Roux, P. C. & Luoto, M. Water as a resource, stress and disturbance shaping tundra vegetation. Oikos 128, 811–822 (2019).
    Google Scholar 
    54.Panchen, Z. A. & Gorelick, R. Canadian arctic archipelago conspecifics flower earlier in the high arctic than the mid-arctic. Int. J. Plant Sci. 177, 661–670 (2016).
    Google Scholar 
    55.Barrett, R. T. & Hollister, R. D. Arctic plants are capable of sustained responses to long-term warming. Polar Res. 35, 1–9 (2016).
    Google Scholar 
    56.Carbognani, M., Bernareggi, G., Perucco, F., Tomaselli, M. & Petraglia, A. Micro-climatic controls and warming effects on flowering time in alpine snowbeds. Oecologia 182, 573–585 (2016).ADS 
    PubMed 

    Google Scholar 
    57.Hollister, R. D., Webber, P. J. & Tweedie, C. E. The response of Alaskan Arctic Tundra to experimental warming: Differences between short- and long-term responses. Glob. Chang. Biol. 11, 525–536 (2005).ADS 

    Google Scholar 
    58.Mulder, C. P. H., Iles, D. T. & Rockwell, R. F. Increased variance in temperature and lag effects alter phenological responses to rapid warming in a subarctic plant community. Glob. Chang. Biol. 23, 801–814 (2017).ADS 
    PubMed 

    Google Scholar 
    59.Marion, G. M. et al. Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob. Chang. Biol. 3, 20–32 (1997).
    Google Scholar 
    60.Walker, M. D. et al. Plant community responses to experimental warming across the tundra biome. Proc. Natl Acad. Sci. USA 103, 1342–1346 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    61.Hollister, R. D. & Webber, P. J. Biotic validation of small open-top chambers in a tundra ecosystem. Glob. Chang. Biol. 6, 835–842 (2000).ADS 

    Google Scholar 
    62.Henry, G. H. R. & Molau, U. Tundra plants and climate change: The International Tundra Experiment (ITEX). Glob. Chang. Biol. 3, 1–9 (1997).ADS 

    Google Scholar 
    63.Welker, J. M., Molau, U., Parsons, A. N., Robinson, C. H. & Wookey, P. A. Responses of Dryas octopetala to ITEX environmental manipulations: a synthesis with circumpolar comparisons. Glob. Chang. Biol. 3, 61–73 (1997).ADS 

    Google Scholar 
    64.Basnett, S., Nagaraju, S. K., Ravikanth, G. & Devy, S. M. Influence of phylogeny and abiotic factors varies across early and late reproductive phenology of Himalayan Rhododendrons. Ecosphere 10, e02581 (2019).65.Panchen, Z. A. et al. Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. N. Phytol. 203, 1208–1219 (2014).CAS 

    Google Scholar 
    66.Davis, C. C., Willis, C. G., Primack, R. B. & Miller-Rushing, A. J. The importance of phylogeny to the study of phenological response to global climate change. Philos. Trans. R. Soc. B Biol. Sci. 365, 3202–3213 (2010).
    Google Scholar 
    67.Hänninen, H. et al. Experiments are necessary in process-based tree phenology modelling. Trends Plant Sci. 24, 199–209 (2019).PubMed 

    Google Scholar 
    68.Hanson, P. J. & Walker, A. P. Advancing global change biology through experimental manipulations: Where have we been and where might we go? Glob. Chang. Biol. 26, 287–299 (2020).ADS 
    PubMed 

    Google Scholar 
    69.Tang, J. et al. Emerging opportunities and challenges in phenology: a review. Ecosphere 7, 1–17 (2016).
    Google Scholar 
    70.Ettinger, A. K. et al. Winter temperatures predominate in spring phenological responses to warming. Nat. Clim. Chang. 10, 1137–1142 (2020).71.Augspurger, C. K. Reconstructing patterns of temperature, phenology, and frost damage over 124 years: Spring damage risk is increasing. Ecology 94, 41–50 (2013).PubMed 

    Google Scholar 
    72.Caradonna, P. J. & Bain, J. A. Frost sensitivity of leaves and fl owers of subalpine plants is related to tissue type and phenology. J. Ecol. 55–64 https://doi.org/10.1111/1365-2745.12482 (2016).73.Gezon, Z. J., Inouye, D. W. & Irwin, R. E. Phenological change in a spring ephemeral: Implications for pollination and plant reproduction. Glob. Chang. Biol. 22, 1779–1793 (2016).ADS 
    PubMed 

    Google Scholar 
    74.Iler, A. M. et al. Reproductive losses due to climate change-induced earlier flowering are not the primary threat to plant population viability in a perennial herb. J. Ecol. 107, 1931–1943 (2019).
    Google Scholar 
    75.CaraDonna, P. J. & Waser, N. M. Temporal flexibility in the structure of plant–pollinator interaction networks. Oikos 129, 1369–1380 (2020).
    Google Scholar 
    76.Fründ, J., Dormann, C. F. & Tscharntke, T. Linné’s floral clock is slow without pollinators – flower closure and plant-pollinator interaction webs. Ecol. Lett. 14, 896–904 (2011).PubMed 

    Google Scholar 
    77.Song, C. & Saavedra, S. Structural stability as a consistent predictor of phenological events. Proc. R. Soc. B Biol. Sci. 285, 20180767 (2018).78.Saavedra, S., Rohr, R. P., Olesen, J. M. & Bascompte, J. Nested species interactions promote feasibility over stability during the assembly of a pollinator community. Ecol. Evol. 6, 997–1007 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    79.Mosbacher, J. B., Michelsen, A., Stelvig, M., Hjermstad-Sollerud, H. & Schmidt, N. M. Muskoxen modify plant abundance, phenology, and nitrogen dynamics in a high Arctic Fen. Ecosystems 22, 1095–1107 (2019).
    Google Scholar 
    80.Barboza, P. S., Van Someren, L. L., Gustine, D. D. & Syndonia Bret-Harte, M. The nitrogen window for arctic herbivores: Plant phenology and protein gain of migratory caribou (Rangifer tarandus). Ecosphere 9, e02073 (2018).81.Gougherty, A. V. & Gougherty, S. W. Sequence of flower and leaf emergence in deciduous trees is linked to ecological traits, phylogenetics, and climate. N. Phytol. 220, 121–131 (2018).
    Google Scholar 
    82.Bjorkman, A. D. et al. Status and trends in Arctic vegetation: evidence from experimental warming and long-term monitoring. Ambio 49, 678–692 (2020).PubMed 

    Google Scholar 
    83.Loe, L. E. et al. The neglected season: Warmer autumns counteract harsher winters and promote population growth in Arctic reindeer. Glob. Chang. Biol. 993–1002 https://doi.org/10.1111/gcb.15458 (2020).84.Ueyama, M. et al. Growing season and spatial variations of carbon fluxes of Arctic and boreal ecosystems in Alaska (USA). Ecol. Appl. 23, 1798–1816 (2013).PubMed 

    Google Scholar 
    85.White, M. A., Running, S. W. & Thornton, P. E. The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Int. J. Biometeorol. 42, 139–145 (1999).86.Natali, S. M. et al. Large loss of CO2 in winter observed across the northern permafrost region. Nat. Clim. Chang. 9, 852–857 (2019).ADS 
    CAS 

    Google Scholar 
    87.Piao, S. et al. Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451, 3–7 (2008).
    Google Scholar 
    88.Radville, L., Post, E. & Eissenstat, D. M. On the sensitivity of root and leaf phenology to warming in the Arctic. Arctic Antarct. Alp. Res. 50, S100020 (2018).89.Sloan, V. L., Fletcher, B. J. & Phoenix, G. K. Contrasting synchrony in root and leaf phenology across multiple sub-Arctic plant communities. J. Ecol. 104, 239–248 (2016).CAS 

    Google Scholar 
    90.Danby, R. K. & Hik, D. S. Responses of white spruce (Picea glauca) to experimental warming at a subarctic alpine treeline. Glob. Chang. Biol. 13, 437–451 (2007).ADS 

    Google Scholar 
    91.Dabros, A., Fyles, J. W. & Strachan, I. B. Effects of open-top chambers on physical properties of air and soil at post-disturbance sites in northwestern Quebec. Plant Soil 333, 203–218 (2010).92.Finger Higgens, R. A. et al. Changing Lake Dynamics indicate a drier Arctic in Western Greenland. J. Geophys. Res. Biogeosci. 124, 870–883 (2019).
    Google Scholar 
    93.Leuzinger, S. et al. Do global change experiments overestimate impacts on terrestrial ecosystems? Trends Ecol. Evol. 26, 236–241 (2011).PubMed 

    Google Scholar 
    94.Molau, U. & MØlgaard, P. ITEX Manual (1996).95.Post, E. et al. The polar regions in a 2 °C warmer world. Sci. Adv. 5, eaaw9883 (2019).96.Cayuela, L., Granzow-de la Cerda, Í., Albuquerque, F. S. & Golicher, D. J. Taxonstand: An r package for species names standardisation in vegetation databases. Methods Ecol. Evol. 3, 1078–1083 (2012).
    Google Scholar 
    97.C3S. ERA5: fifth generation of ECMWF atmospheric reanalyses of the global climate. Copernicus Climate Change Service (C3S) Climate Data Store (CDS). https://cds.climate.copernicus.eu/cdsapp#!/home%0A (2017).98.Kittel, T. G. F. et al. Contrasting long-term alpine and subalpine precipitation trends in a mid-latitude North American mountain system, Colorado Front Range, USA. Plant Ecol. Divers. 8, 607–624 (2015).
    Google Scholar 
    99.Therneau, T. A package for survival analysis in S. Citeseer 1–83 (2020).100.R Core Team. R: A Language and Environment for Statistical Computing (2019).101.Bürkner, P.-C. brms: An R package for bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).102.van de Pol, M. & Wright, J. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77, 753–758 (2009).
    Google Scholar 
    103.Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences linked references are available on JSTOR for this article: inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).MATH 

    Google Scholar 
    104.Makowski, D., Ben-Shachar, M. & Lüdecke, D. bayestestR: describing effects and their uncertainty, existence and significance within the Bayesian framework. J. Open Source Softw. 4, 1541 (2019).ADS 

    Google Scholar 
    105.Pebesma, E. Simple features for R: standardized support for spatial vector data. R J 10, 439–446 (2018).
    Google Scholar 
    106.Wickham, H. Elegant Graphics for Data Analysis Media Vol. 35 (Springer Publishing Company, Incorporated, 2009).107.Collins, C. cour10eygrace/OTC_synthesis_analyses: release for Nature Communications manuscript (Version v1.0.3). Zenodo https://doi.org/10.5281/zenodo.4763165 (2021). More

  • in

    Southward decrease in the protection of persistent giant kelp forests in the northeast Pacific

    Mapping kelp persistenceThe study area for this analysis encompasses the region where Macrocystis pyrifera is the dominant canopy kelp species in the Northeast Pacific Ocean. The region extends from Año Nuevo Island in the north (latitude ~37.1°), California, USA, to Punta Prieta in the south (latitude ~27°), Baja California Sur, Mexico. We mapped the distribution of giant kelp canopy and characterized persistence using a 30-m resolution satellite-based time series covering our entire study area27. These data provide quarterly estimates of kelp canopy area across the study region from 1984 to 2018. We estimated giant kelp canopy from three Landsat sensors: Landsat 5 Thematic Mapper (1984–2011), Landsat 7 Enhanced Thematic Mapper+ (1999–present), and Landsat 8 Operational Land Imager (2013–present). We downloaded all imagery as atmospherically corrected Landsat Collection 1 Level-2 products. Each Landsat sensor has a pixel resolution of 30 × 30 m and a repeat time of 16 days (8 days when two Landsat sensors were operational). Since Landsat imagery can be obscured by cloud cover, we obtained a clear estimate of kelp areas ~16 times per year from 1984 to 2018 (mean = 16.2, std = 4.1). The repeated observations across the time series avoid missing kelp canopy due to physical processes such as tides and currents. Multiple Landsat passes over seasonal timescales are successful at mitigating the effect of tide and tidal currents on Landsat kelp canopy detection27.While the pixel resolution of Landsat sensors is 30 × 30 m, we were able to observe the presence and density of kelp canopy on subpixel scales using a fully automation procedure. We first masked all land areas using a global 30 m resolution digital elevation model (asterweb.jpl.nasa. gov/gdem.asp) and classified the remaining pixels as seawater, cloud, or kelp canopy using a binary decision tree classifier trained on a diverse array of pixels within the study region27. We then used Multiple Endmember Spectral Mixture Analysis39 to model each pixel as the linear combination of seawater and kelp canopy. This method can accurately obtain kelp canopy presence as long as kelp canopy covers ~13% of a 30 m pixel. These methods were validated using 15 years of monthly kelp canopy surveys by the Santa Barbara Coastal Long Term Ecological Research project at two sites in Southern California. We filtered errors of commission (such as free-floating kelp paddies) by removing any pixels classified as kelp canopy in More