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    Bird-feeder cleaning lowers disease severity in rural but not urban birds

    1.Vitousek, P. M., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).CAS 
    Article 

    Google Scholar 
    2.Galvani, A. P., Bauch, C. T., Anand, M., Singer, B. H. & Levin, S. A. Human-environment interactions in population and ecosystem health. Proc. Natl. Acad. Sci. U.S.A. 113, 14502–14506 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Robb, G. N., McDonald, R. A., Chamberlain, D. E. & Bearhop, S. Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front. Ecol. Environ. 6, 476–484 (2008).Article 

    Google Scholar 
    4.Wilcoxen, T. E. et al. Effects of bird-feeding activities on the health of wild birds. Conserv. Physiol. 3, 058 (2015).Article 
    CAS 

    Google Scholar 
    5.Oro, D., Genovart, M., Tavecchia, G., Fowler, M. S. & Martinez-Abrain, A. Ecological and evolutionary implications of food subsidies from humans. Ecol. Lett. 16, 1501–1514 (2013).PubMed 
    Article 

    Google Scholar 
    6.Jones, D. An appetite for connection: Why we need to understand the effect and value of feeding wild birds. Emu 111, 1–7 (2011).Article 

    Google Scholar 
    7.Hanmer, H. J., Thomas, R. L. & Fellowes, M. D. E. Provision of supplementary food for wild birds may increase the risk of local nest predation. Ibis 159, 158–167 (2017).Article 

    Google Scholar 
    8.Malpass, J. S., Rodewald, A. D. & Matthews, S. N. Species-dependent effects of bird feeders on nest predation and nest survival of urban American robins and northern cardinals. Condor 119, 1–16 (2017).Article 

    Google Scholar 
    9.Loss, S. R. & Marra, P. P. Population impacts of free-ranging domestic cats on mainland vertebrates. Front. Ecol. Environ. 15, 502–509 (2017).Article 

    Google Scholar 
    10.Jones, D. N. & Reynolds, S. J. Feeding birds in our towns: A global research opportunity. J. Avian Biol. 39, 265–271 (2008).Article 

    Google Scholar 
    11.Adelman, J. S., Moyers, S. C., Farine, D. R. & Hawley, D. M. Feeder use predicts both acquisition and transmission of a contagious pathogen in a North American songbird. Proc. R. Soc. B 282, 20151429 (2015).PubMed 
    Article 

    Google Scholar 
    12.Becker, D. J., Hall, R. J., Forbes, K. M., Plowright, R. K. & Altizer, S. Anthropogenic resource subsidies and host-parasite dynamics in wildlife. Phil. Trans. R. Soc. B 373, 20170086 (2018).PubMed 
    Article 

    Google Scholar 
    13.Becker, D. J., Streicker, D. G. & Altizer, S. Linking anthropogenic resources to wildlife–pathogen dynamics: A review and meta-analysis. Ecol. Lett. 18, 483–495 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    14.Dhondt, A. A., Dhondt, K. V., Hawley, D. M. & Jennelle, C. S. Experimental evidence for transmission of Mycoplasma gallisepticum in house finches by fomites. Avian Pathol. 36, 205–208 (2007).PubMed 
    Article 

    Google Scholar 
    15.Pierce II, R. A. & Denkler, S. Attracting hummingbirds to your property. In Agricultural Guides—University of Missouri-Columbia Extension, Vol. g9419 (2016). https://extensiondata.missouri.edu/pub/pdf/agguides/wildlife/g09419.pdf. Accessed 22 May 2020.16.Patterson, S., Janke, A., Bryan, G., Pease, J. & Jungbluth, K. Attracting Birds to Your Yard Vol. 219 (Iowa State Extension and Outreach Publications, 2017).
    Google Scholar 
    17.Feliciano, L. M., Underwood, T. J. & Aruscavage, D. F. The effectiveness of bird feeder cleaning methods with and without debris. Wilson J. Ornithol. 130, 313–320 (2018).Article 

    Google Scholar 
    18.Faustino, C. R. et al. Mycoplasma gallisepticum infection dynamics in a house finch population: Seasonal variation in survival, encounter and transmission rate. J. Anim. Ecol. 73, 651–669 (2004).Article 

    Google Scholar 
    19.Thompson, C. W., Hillgarth, N., Leu, M. & McClure, H. E. High parasite load in house finches (Carpodacus mexicanus) is correlated with expression of a sexually selected trait. Am. Nat. 149, 270–294 (1997).Article 

    Google Scholar 
    20.Chace, J. F. & Walsh, J. J. Urban effects on native avifauna: A review. Landsc. Urban Plann. 74, 46–69 (2006).Article 

    Google Scholar 
    21.Bradley, C. A. & Altizer, S. Urbanization and the ecology of wildlife diseases. Trends Ecol. Evol. 22, 95–102 (2007).PubMed 
    Article 

    Google Scholar 
    22.Giraudeau, M., Mousel, M., Earl, S. & McGraw, K. J. Parasites in the city: Degree of urbanization predicts poxvirus and coccidian infections in house finches (Haemorhous mexicanus). PLoS ONE 9, e86747 (2014).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    23.Hasegawa, M., Ligon, R. A., Giraudeau, M., Watanabe, M. & McGraw, K. J. Urban and colorful male house finches are less aggressive. Behav. Ecol. 25, 641–649 (2014).Article 

    Google Scholar 
    24.Giraudeau, M., Toomey, M. B., Hutton, P. & McGraw, K. J. Expression of and choice for condition-dependent carotenoid-based color in an urbanizing context. Behav. Ecol. 29, 1307–1315 (2018).
    Google Scholar 
    25.Hill, G. E. A Red Bird in a Brown Bag: The Function and Evolution of Colorful Plumage in the House Finch (Oxford University Press, 2002).Book 

    Google Scholar 
    26.Pyle, P. Identification Guide to North American Birds, Part I (Slate Creek Press, 1997).
    Google Scholar 
    27.Brawner, W. R., Hill, G. E. & Sundermann, C. A. Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male house finches. Auk 117, 952–963 (2000).Article 

    Google Scholar 
    28.Dolnik, O. V., Dolnik, V. R. & Bairlein, F. The effect of host foraging ecology on the prevalence and intensity of coccidian infection in wild passerine birds. Ardea 98, 97–103 (2010).Article 

    Google Scholar 
    29.Pierson, F. W., Larsen, C. T. & Gross, W. B. The effect of stress on the response of chickens to coccidiosis vaccination. Vet. Parasitol. 73, 177–180 (1997).CAS 
    PubMed 
    Article 

    Google Scholar 
    30.Hõrak, P. et al. How coccidian parasites affect health and appearance of greenfinches. J. Anim. Ecol. 73, 935–947 (2004).Article 

    Google Scholar 
    31.Surmacki, A. & Hill, G. E. Coccidia infection does not influence preening behavior in American goldfinches. Acta Ethol. 17, 107–111 (2014).PubMed 
    Article 

    Google Scholar 
    32.Staley, M., Bonneaud, C., McGraw, K. J., Vleck, C. M. & Hill, G. E. Detection of Mycoplasma gallisepticum in house finches (Haemorhous mexicanus) from Arizona. Avian Dis. 62, 14–17 (2017).Article 

    Google Scholar 
    33.R Core Team. R: A language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2016). https://www.R-project.org/. Accessed 22 May 2020.34.Nolan, P. M., Hill, G. E. & Stoehr, A. M. Sex, size, and plumage redness predict house finch survival in an epidemic. Proc. R. Soc. B 265, 961–965 (1998).Article 

    Google Scholar 
    35.Hutton, P., Wright, C. D., DeNardo, D. F. & McGraw, K. J. No effect of human presence at night on disease, body mass, or metabolism in rural and urban house finches (Haemorhous mexicanus). Integr. Comp. Biol. 58, 977–985 (2018).PubMed 

    Google Scholar 
    36.Giraudeau, M. & McGraw, K. J. Physiological correlates of urbanization in a desert songbird. Integr. Comp. Biol. 54, 622–632 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Cook, M. O., Weaver, M. J., Hutton, P. & McGraw, K. J. The effects of urbanization and human disturbance on problem solving in juvenile house finches (Haemorhous mexicanus). Behav. Ecol. Sociobiol. 71, 85 (2017).Article 

    Google Scholar 
    38.Moyers, S. C., Adelman, J. S., Farine, D. R., Thomason, C. A. & Hawley, D. M. Feeder density enhances house finch disease transmission in experimental epidemics. Philos. Trans. R. Soc. B 373, 20170090 (2018).Article 
    CAS 

    Google Scholar 
    39.Boyd, M. L., Underwood, T. J. & Aruscavage, D. F. The efficacy of cleaning bird feeders with 10% bleach wipes to reduce bacteria. J. Pennsyl. Acad. Sci. 88, 220–226 (2014).
    Google Scholar 
    40.Belthoff, J. R. & Gowaty, P. A. Male plumage coloration affects dominance and aggression in female house finches. Bird Behav. 11, 1–7 (1996).Article 

    Google Scholar 
    41.Zylberberg, M., Klasing, K. C. & Hahn, T. P. House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biol. Lett. 9, 20120856 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Sykes, B. E., Hutton, P. & McGraw, K. J. Sex-specific relationships between urbanization, parasitism, and plumage coloration in house finches. Curr. Zool. https://doi.org/10.1093/cz/zoaa060 (2020).Article 

    Google Scholar 
    43.McGraw, K. J. & Ardia, D. R. Sex differences in carotenoid status and immune performance in zebra finches. Evol. Ecol. Res. 7, 251–262 (2005).
    Google Scholar 
    44.Bailly, J. et al. Negative impact of urban habitat on immunity in the great tit Parus major. Oecologia 182, 1053–1062 (2016).PubMed 
    Article 
    ADS 

    Google Scholar 
    45.Badyaev, A. V., Belloni, V. & Hill, G. E. House finch (Haemorhous mexicanus), version 1.0. In Birds of the World (ed. Poole, A. F.) (Cornell Lab of Ornithology, 2020).
    Google Scholar 
    46.Thompson, W. L. Agonistic behavior in the house finch. Part I: Annual cycle and display patterns. Condor 62, 245–271 (1960).Article 

    Google Scholar 
    47.Hotchkiss, E. R., Davis, A. K., Cherry, J. J. & Altizer, S. Mycoplasmal conjunctivitis and the behavior of wild house finches (Carpodacus mexicanus) at bird feeders. Bird Behav. 17, 1–8 (2005).
    Google Scholar  More

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    Maintenance power requirements of anammox bacteria “Candidatus Brocadia sinica” and “Candidatus Scalindua sp.”

    1.Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MCM. Full-scale partial nitritation/anammox experience – an application survey. Water Res. 2014;55:292–303.CAS 
    PubMed 
    Article 

    Google Scholar 
    2.Ali M, Okabe S. Anammox-based technologies for nitrogen removal: Advances in process start-up and remaining issues. Chemosphere. 2015;141:144–53.CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Ni S, Sung S, Yue Q, Gao B. Substrate removal evaluation of granular anammox process in a pilot-scale upflow anaerobic sludge blanket reactor. Ecol Eng 2012;38:30–36.Article 

    Google Scholar 
    4.Wang B, Peng Y, Guo Y, Yuan Y, Zhao M, Wang S. Impact of partial nitritation degree and C/N ratio on simultaneous sludge fermentation, denitrification and anammox process. Bioresour Technol. 2016;219:411–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Zhang L, Narita Y, Gao L, Ali M, Oshiki M, Okabe S. Maximum specific growth rate of anammox bacteria revisited. Water Res. 2017;116:296–303.CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Zhang L, Okabe S. Ecological niche differentiation among anammox bacteria. Water Res. 2020;171:115468.CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Sun W, Xu MY, Wu WM, Guo J, Xia CY, Sun GP, et al. Molecular diversity and distribution of anammox community in sediments of the Dongjiang River, a drinking water source of Hong Kong. J Appl Microbiol. 2014;116:464–76.CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Zhu GB, Wang SY, Wang WD, Wang Y, Zhou LL, Jiang B, et al. Hotspots of anaerobic ammonium oxidation at land-freshwater interfaces. Nat Geosci. 2013;6:103–7.CAS 
    Article 

    Google Scholar 
    9.Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA. 2005;102:6478–83.CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Schmid M, Risgaard-Petersen N, van de Vossenberg J, Kuypers MMM, Lavik G, Petersen J, et al. Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol. 2007;9:1476–84.CAS 
    PubMed 
    Article 

    Google Scholar 
    11.Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuña-González J. N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature. 2003;422:606–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Kuypers MMM, Olav Sliekers A, Lavik G, Schmid M, Jørgensen BB, Gijs Kuenen J, et al. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature. 2003;422:608–11.CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J. Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J. 2010;4:450–4.PubMed 
    Article 

    Google Scholar 
    14.Zhu GB, Wang SY, Wang Y, Wang CX, Risgaard-Petersen N, Jetten MSM, et al. Anaerobic ammonia oxidation in a fertilized paddy soil. ISME J. 2011;5:1905–12.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Oshiki M, Satoh H, Okabe S. Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ Microbiol. 2016;18:2784–96.CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Sonthiphand P, Hall MW, Neufeld JD. Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Front Microbiol. 2014;5:1–14.Article 

    Google Scholar 
    17.van Bodegom P. Microbial maintenance: A critical review on its quantification. Microb Ecol. 2007;53:513–23.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Wang G, Post WM. A theoretical reassessment of microbial maintenance and implications for microbial ecology modeling. FEMS Microbiol Ecol. 2012;81:610–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Overkamp W, Ercan O, Herber M, van Maris AJA, Kleerebezem M, Kuipers OP. Physiological and cell morphology adaptation of Bacillus subtilis at near-zero specific growth rates: a transcriptome analysis. Environ Microbiol. 2015;17:346–63.PubMed 
    Article 

    Google Scholar 
    20.Ma X, Wang Y, Zhou S, Yan Y, Lin X, Wu M. Endogenous metabolism of anaerobic ammonium oxidizing bacteria in response to short-term anaerobic and anoxic starvation stress. Chem Eng J. 2017;313:1233–41.CAS 
    Article 

    Google Scholar 
    21.Ma X, Wang Y. Anammox bacteria exhibit capacity to withstand long-term starvation stress: a proteomic-based investigation of survival mechanisms. Chemosphere. 2018;211:952–61.CAS 
    PubMed 
    Article 

    Google Scholar 
    22.Xing B-S, Guo Q, Jiang X-Y, Chen Q-Q, He M-M, Wu L-M, et al. Long-term starvation and subsequent reactivation of anaerobic ammonium oxidation (anammox) granules. Chem Eng J. 2016;287:575–84.CAS 
    Article 

    Google Scholar 
    23.Wang Q, Song K, Hao X, Wei J, Pijuan M, van Loosdrecht MCM, et al. Evaluating death and activity decay of Anammox bacteria during anaerobic and aerobic starvation. Chemosphere. 2018;201:25–31.CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Lopez C, Pons MN, Morgenroth E. Endogenous processes during long-term starvation in activated sludge performing enhanced biological phosphorous removal. Water Res. 2006;40:1519–30.CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Tappe W, Laverman A, Bohland M, Braster M, Rittershaus S, Groeneweg J, et al. Maintenance energy demand and starvation recovery dynamics of Nitrosomonas europaea and Nitrobacter winogradskyi cultivated in a retentostat with complete biomass retention. Appl Environ Microbiol. 1999;65:2471–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    26.Vos T, Hakkaart XDV, de Hulster EAF, van Maris AJA, Pronk JT, Daran-Lapujade P. Maintenance-energy requirements and robustness of Saccharomyces cerevisiae at aerobic near-zero specific growth rates. Micro Cell Fact. 2016;15:111.Article 
    CAS 

    Google Scholar 
    27.Ali M, Oshiki M, Awata T, Isobe K, Kimura Z, Yoshiaki H, et al. Physiological characterization of anaerobic ammonium oxidizing bacterium “Candidatus Jettenia caeni”. Environ Microbiol. 2015;17:2172–89.CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Narita Y, Zhang L, Kimura, Ali M, Fujii T, Okabe S. Enrichment and physiological characterization of an anaerobic ammonium-oxidizing bacterium “Candidatus Brocadia sapporoensis”. Syst Appl Microbiol. 2017;40:448–57.CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Oshiki M, Shimokawa M, Fujii N, Satoh H, Okabe S. Physiological characteristics of the anaerobic ammonium-oxidizing bacterium “Candidatus Brocadia sinica”. Microbiol. 2011;157:1706–13.CAS 
    Article 

    Google Scholar 
    30.Okabe, S, Shafdar, AA, Kobayashi, K, Zhang, L, and Oshiki, M. Glycogen metabolism of the anammox bacterium “Candidatus Brocadia sinica” ISME J. 2020; https://doi.org/10.1038/s41396-020-00850-5.31.van der Star WRL, Miclea AI, van Dongen UGJM, Muyzer G, Picioreanu C, van Loosdrecht MCM. The membrane bioreactor: a novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng. 2008;101:286–94.PubMed 
    Article 
    CAS 

    Google Scholar 
    32.Zhang L, Okabe S. Rapid cultivation of free-living planktonic anammox cells. Water Res. 2017;127:204–10.CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Oshiki M, Awata T, Kindaichi T, Satoh H, Okabe S. Cultivation of planktonic anaerobic ammonium oxidation (Anammox) bacteria using membrane bioreactor. Microbes Environ. 2013;28:436–43.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Awata T, Oshiki M, Kindaichi T, Ozaki N, Ohashi A, Okabe S. Physiological characterization of an anaerobic ammonium-oxidizing bacterium belonging to the “Candidatus Scalindua” group. Appl Environ Microbiol. 2013;79:4145–8.CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Zhang L, Narita Y, Gao L, Ali M, Oshiki M, Ishii S, et al. Microbial competition among anammox baxteria in nitrite-limited bioreactors. Water Res. 2017;125:249–58.CAS 
    PubMed 
    Article 

    Google Scholar 
    36.Graaf AA, Van DE, Bruijn PDE, Robertson LA, Jetten MSM, Kuenen JG. Autotrophic growth of anaerobic in a fluidized bed reactor. Microbiol. 1996;142:2187–96.Article 

    Google Scholar 
    37.Kindaichi T, Awata T, Suzuki Y, Tanabe K, Hatamoto M, Ozaki N, et al. Enrichment using an up-flow column reactor and community structure of marine anammox bacteria from coastal sediment. Microbes Environ. 2011;26:67–73.PubMed 
    Article 

    Google Scholar 
    38.APHA. Standard Methods for the Examination of Water and Sewage, Washington DC,1998,39.Nagaraja P, Shivaswamy M, Kumar H. Highly sensitive N-(1-Naphthyl)ethylene diamine method for the spectrophotometric determination of trace amounts of nitrite in various water samples. Intern J Environ Anal Chem. 2001;80:39–48.CAS 
    Article 

    Google Scholar 
    40.Tsushima I, Ogasawara Y, Kindaichi T, Satoh H, Okabe S. Development of high-rate anaerobic ammonium-oxidizing (anammox) biofilm reactors. Water Res. 2007;41:1623–34.CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Kindaichi T, Tsushima I, Ogasawara Y, Shimokawa M, Ozaki N, Satoh H, et al. In situ activity and spatial organization of anaerobic ammonium-oxidizing (anammox) bacteria in biofilms. Appl Environ Microbiol. 2007;73:4931–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Okabe S, Satoh H, Watanabe Y. In situ analysis of nitrifying biofilms as determined by in situ hybridization and the use of microelectrodes. Appl Environ Microbiol. 1999;65:3182–91.CAS 
    PubMed 
    Article 

    Google Scholar 
    43.Pirt SJ. Maintenance energy of bacteria in growing cultures. Proc R soc Lond B Biol Sci. 1965;163:224–31.CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Pirt SJ. Maintenance energy: a general model for energy-limited and energy-sufficient growth. Arch Microbiol. 1982;133:300–2.CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Herbert D, Elsworth R, Telling RC. The continuous culture of bacteria: a theoretical and experimental study. J Gen Microbiol. 1956;14:601–22.CAS 
    PubMed 
    Article 

    Google Scholar 
    46.van Verseveld HW, De Hollander JA, Frankena J, Braster M, Leeuwerik FJ, Stouthamer AH. Modeling of microbial substrate conversion, growth and product formation in a recycling fermentor. Antonie Van Leeuwenhoek. 1986;52:325–42.PubMed 
    Article 

    Google Scholar 
    47.Lotti T, Kleerebezem R, Lubello C, van Loosdrecht MCM. Physiological and kinetic characterization of a suspended cell anammox culture. Water Res. 2014;60:1–14.CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Tijhuis L, Van Loosdrecht MCM, Heijnen JJ. A thermodynmically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol Bioeng. 1993;42:509–19.CAS 
    PubMed 
    Article 

    Google Scholar 
    49.Strous M, Heijnen JJ, Kuenen JG, Jetten MSM. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol. 1998;50:589–96.CAS 
    Article 

    Google Scholar 
    50.Awata T, Kindaichi T, Ozaki N, Ohashi A. Biomass yield efficiency of the marine anammox bacterium, “Candidatus Scalindua sp.,” is affected by salinity. Microbes Environ. 2015;30:86–91.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Henze, M. Wastewater Treatment: Biological and chemical processes. New York, NY: Springer, 1997.52.Vandekerckhove, TGL, Bodé, S, De Mulder, C, Vlaeminck, SE, Boon, N. 13C Incorporation as a tool to estimate biomass yields in thermophilic and mesophilic nitrifying communities. Front Microbiol. 2019;10:192.53.Tappe W, Tomaschewski C, Rittershaus S, Groeneweg J. Cultivation of nitrifying bacteria in the retentostat, a simple fermentor with internal biomass retention. FEMS Microbiol Ecol. 1996;19:47–52.CAS 
    Article 

    Google Scholar 
    54.Rebnegger C, Vos T, Graf AB, Valli M, Pronk JT, Daran-Lapujade P, et al. Picha pastoris exhibits high viability and a low maintenance energy requirement at near-zero specific growth rates. Appl Environ Microbiol. 2016;82:4570–83.CAS 
    PubMed 
    Article 

    Google Scholar 
    55.Lever MA, Rogers KL, Lloyd KG, Overmann J, Schink B, Thauer RK, et al. Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations. FEMS Microbiol Rev. 2015;39:688–728.CAS 
    PubMed 
    Article 

    Google Scholar 
    56.Bulthuis BA, Frankena J, Koningstein GM, van Verseveld HW, Stouthamer AH. Instability of protease production in a rel1/rel2 pair of Bacillus licheniformis and associated morphological and physiological characteristics. Antonie Leeuwenhoek. 1988;54:95–111.CAS 
    PubMed 
    Article 

    Google Scholar 
    57.Kempes, CP, van Bodegom PM, Wolpert, D, Libby, E, Amend, J, Hoehler, T. Drivers of bacterial maintenance and minimal energy requirements. Front Microbiol. 2017;8:31.58.Amend JP, Shock EL. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev. 2001;25:175–243.CAS 
    PubMed 
    Article 

    Google Scholar 
    59.Amend JP, LaRowe DE. Minireview: demystifying microbial reaction energetics. Environ Microbiol. 2019;21:3539–47.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Kartal B, Keltjens JT. Anammox biochemistry: a tale of heme c proteins. Trends Biochem Sci. 2016;41:998–1011.CAS 
    PubMed 
    Article 

    Google Scholar 
    61.Scholten JCM, Conrad R. Energetics of syntrophic propionate oxidation in defined batch and chemostat coculture. Appl Environ Microbiol. 2000;66:2934–42.CAS 
    PubMed 
    Article 

    Google Scholar 
    62.LaRowe DE, Amend JP. The energetics of anabolism in natural settings. ISME J. 2016;10:1285–95.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    63.LaRowe DE, Amend JP. Catabolic rates, population sizes and doubling/replacement times of microorganisms in natural settings. Am J Sci. 2015;315:167–203.CAS 
    Article 

    Google Scholar 
    64.Marschall E, Jogler M, Henssge U, Overmann J. Large-scale distribution and activity patterns of an extremely low-light-adapted population of green sulfur bacteria in the Black Sea. Environ Microbiol. 2010;12:1348–62.CAS 
    PubMed 
    Article 

    Google Scholar 
    65.Bradley, JA, Arndt, S, Amend, JP, Burwicz, E, Dale, AW, Egger, M et al. Widespread energy limitation to life in global subseafloor sediments. Sci Adv. 2020;6:eaba0697.66.Hoehler TM, Jorgensen BB. Microbial life under extreme energy limitation. Nat Rev Microbiol. 2013;11:83–94.CAS 
    PubMed 
    Article 

    Google Scholar 
    67.LaRowe, DE, Amend, JP. Power limits for microbial life. Front Microbiol 2015;6:718.68.Zhao R, Mogollon JM, Abby SS, Schleper C, Biddle JF, Roerdink DL. et al. Geochemical transition zone powering microbial growth in subsurface sediments. Proc Natl Acad Sci USA. 2020;117:32617–26.CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Pitcher A, Villanueva L, Hopmans EC, Schouten S, Reichart G-J, Sinninghe Damste JS. Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J. 2011;5:1896–904.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    70.Füssel J, Lam P, Lavik G, Jensen MM, Holtappels M, Günter M, et al. Nitrite oxidation in the Namibian oxygen minimum zone. ISME J. 2012;6:1200–9.PubMed 
    Article 
    CAS 

    Google Scholar 
    71.Füchslin HP, Schneider C, Egli T. In glucose-limited continuous culture the minimum substrate concentration for growth, Smin, is crucial in the competition between the enterobacterium Escherichia coli and Chelatobacter heintzii, an environmentally abundant bacterium. ISME J. 2012;6:777–89.PubMed 
    Article 
    CAS 

    Google Scholar  More

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    Russian forest sequesters substantially more carbon than previously reported

    Russia has been reporting almost no changes in forested area, growing stock volume (GSV) and biomass to the United Nations Framework Convention on Climate Change (UNFCCC)1 and the Food and Agriculture Organization of the United Nations (FAO) Forest Resources Assessment (FRA)2 since the collapse of the USSR and the decline in the Soviet Forest Inventory and Planning (FIP) system. According to the State Forest Register (SFR)3, which is the main repository of forest information, and national reporting to the FAO FRA2, the GSV and the above ground biomass (AGB) increased by 1.1% and 0.6% (Table S1), respectively, during 1990–2015, yet studies using remote sensing (RS) indicate increased vegetation productivity4, tree cover (annual rate + 0.417% over 1982–2016)5, increased AGB (+ 329 Tg C yr−1 over 2000–20076), total biomass (annual rate + 0.44% or + 153 Tg C yr−1 over 1990–20077), and forest ecosystem carbon pools (ca + 470 Tg C yr−1 over 2001–20198). This inconsistency in estimates can be explained by an information gap that appeared when Russia decided to move from the FIP to another system for the collection of forest information at the national scale – the National Forest Inventory (NFI).The FIP involves revisiting every forest stand (on the ground for managed forests or using RS techniques for remote non-commercial forests) on a 10–15-year interval, with the measurement of forest parameters combined with the formulation of forest management directives. After the collapse of the USSR, the inventory within the FIP system slowed down substantially. For example, more than 50% of the forest area was surveyed by the FIP more than 25 years ago9. For these reasons, the reliability of information on forests in Russia has deteriorated since 1988, which is the year when FIP-based reporting10 involved the largest inventory efforts in recent decades. According to this report10, the total GSV of Russian forests was 81.7 × 109 m3 (without shrubland, bias corrected11). This value is used here as a reference to quantify biomass stock changes in Russia with respect to the current decade.In contrast, NFI is a state-of-the-art inventory system based on a statistical sampling method. It was initiated in 2007 and the first cycle was completed in 2020. The NFI data processing is ongoing, but the first official press release12 suggests that Russian forest accumulated 102 × 109 m3 over its lifespan until 2014. Once finalized, the NFI will be verified before adoption as the official source of information to the SFR and national reporting. The NFI has received some criticism13 because of the relatively sparse sampling employed and the stratification method used, which is partially based on outdated FIP data.In Russia, the long intervals between consecutive surveys and the difficulty in accessing very remote regions in a timely manner by an inventory system make satellite RS an essential tool for capturing forest dynamics and providing a comprehensive, wall-to-wall perspective on biomass distribution. However, observations from current RS sensors are not suited for producing accurate biomass estimates unless the estimation method is calibrated with a dense network of measurements from ground surveys14. Here we calibrated models relating two global RS biomass data products (GlobBiomass GSV15 and CCI Biomass GSV16) and additional RS data layers (forest cover mask9, the Copernicus Global Land Cover CGLS‐LC100 product17) with ca 10,000 ground plots (see Material and Methods) to reduce nuances in the individual input maps due to imperfections in the RS data and approximations in the retrieval procedure18,19. The combination of these two sources of information, i.e., ground measurements and RS, utilizes the advantages of both sources in terms of: (i) highly accurate ground measurements and (ii) the spatially comprehensive coverage of RS products and methods. The amount of ground plots currently available may be insufficient for providing an accurate estimate of GSV for the country when used alone, but they are the key to obtaining unbiased estimates when used to calibrate RS datasets20. The map merging procedure was preferred over a plot-aided direct estimation of GSV or AGB from the RS data because of the usually poor association between biomass measured at inventory plots and remote sensing observables21. In addition, models relating biomass and remote sensing observables that are trained with spatially inhomogeneous datasets (Figure S1) tend to be biased in regions not represented by the dataset of the reference biomass measurements.We estimate the total GSV of Russia for the year 2014 for the official forested area (713.1 × 106 ha) to be 111 ± 1.3 × 109 m3, which is 39% higher than the 79.9 × 109 m3 (excluding shrubland) figure reported in the SFR3 for the same year. An additional 7.1 × 109 m3 or 9% were found due to the larger forested area (+ 45.7 106 ha) recognized by RS9, following the expansion of forests to the north22, to higher elevations, in abandoned arable land23, as well as the inclusion of parks, gardens and other trees outside of forest, which were not counted as forest in the SFR. Based on cross-validation, our estimate at the regional level (81 regions of Russia – Table S2, Figure S2) is unbiased. The standard error varied from 0.6 to 17.6% depending on the region. The median error was 1.6%, while the area weighted error was 1.2%. The predicted GSV (Fig. 1) with associated uncertainties is available here (https://doi.org/10.5281/zenodo.3981198) as a GeoTiff at a spatial resolution of 3.2 arc sec. (ca 0.5 ha).Figure 1Predicted mean forest growing stock volume (m3 ha-1) for the year ca 2014 (Generated by Esri ArcGIS Desktop v.10.7, URL: https://desktop.arcgis.com/en/arcmap/).Full size imageHoughton et al.24 estimated forest biomass based on RS and FIP data in Russia for the year 2000. Average forest biomass density varied between 80.6 and 88.2 Mg ha-1 depending on which forest mask was used. Our estimate for the year 2014 of 107 Mg ha-1 (using the conversion factor of GSV to AGB from24 0.6859) is 21–33% higher than the one by Houghton et al., but this is consistent with expected biomass increases over time, i.e., 14 years after the Houghton et al. estimate.Assuming an unchanged total forest area (721.7 × 106 ha) in 1988 and 2014, we conclude that Russian forests have accumulated 1,163 × 106 m3 yr-1 or 407 Tg C yr-1 in live biomass of trees on average over 26 years. This gives an average GSV change rate of + 1.61 m3 ha-1 yr-1 or + 0.56 t C ha-1 yr-1. The sequestration rate obtained, however, should be treated with caution because different methods have been applied in 1988 and 2014 (see “Caveats and Limitations” section). To provide some context for the magnitude of these numbers, one can compare the Russian forest gain to the net GSV losses in tropical forests over the period 1990–2015 according to FAO FRA25 (-1,033 × 106 m3 yr-1 in the regions with a negative trend: South and Central America, South and Southeast Asia, and Africa). A similar divergence in the carbon sink between Tropical and Boreal forest was recognized by Tagesson et al.26.In terms of carbon stock change, our estimates are substantially higher than those reported by Pan et al.7 for 1990–2007 (+ 153 Tg C yr-1) based on FIP data. The biomass carbon estimates by Liu et al.6 are instead in line with our results. There is an increase in the annual rate of AGB in Russia of + 329 Tg C yr−1 (annual variation from 214 to 400 Tg C yr−1) over 2000–20076. Interestingly, another boreal country – Canada – has demonstrated neutral or negative trends (from 0 to -14 Tg C yr−1) for the same time span using the same estimation method6.We can observe different spatial patterns in the change in the GSV density between 1988 (FIP10, bias corrected11) and 2014 (our estimate), which can be explained by climate change, CO2 fertilisation and changes in disturbance regimes (Fig. 2). The average linear trend in the annual temperature increase during 1976–2014 in Russia is + 0.45 °C per 10 years27. The temperature increase is statistically significant in every region except for western Siberia (Fig. 2–3). Significantly increased temperature extremes and an increase in the number of days without precipitation is observed in the south of European Russia, Baikal, Kamchatka, and Chukotka27 (Fig. 2–1). Some regions in the south of the European part of Russia are colored in dark blue, but they, as a rule, have a small share of forested area, which is often linked to water bodies and, therefore, suffers less from increased drought (Fig. 2–1). Central and eastern Siberia suffer from an increase in disturbances, which offsets the climate stimulation effect (Fig. 2–4). The forested area in the Nenets region (Fig. 2–2) is 4 times larger in 2014 based on the RS forest mask compared to the SFR in 1988 (where forest was accounted for up until a certain latitude at that time), where the increase in area resulted in a decrease in the average GSV.Figure 2Change in growing stock volume (m3 ha-1) from 1988 to 2014 (average over administrative regions) (Generated by Esri ArcGIS Desktop v.10.7, URL: https://desktop.arcgis.com/en/arcmap/). These changes can be categorized into: 1—significant increase in air temperature and drought; 2—substantially increased forest area, which lowers the average GSV density; 3—least (not significant) temperature increase; 4—increase of disturbances: wildfire and harvest (southern part), which offsets the climate stimulation effect.Full size imageFocusing specifically on national reporting of managed forest to the UNFCCC, 72% of forested area in Russia is considered to be managed1. We multiplied the GSV density by the managed forest area for each administrative region (Table S3). The difference in GSV estimation (between ours and the one from the SFR report) is 23.6 × 109 m3 (Table S3) or 33% higher. From the GSV of managed forests in 2014 and based on the same area in 1988, we can estimate the sequestration rate of live biomass of managed forests as 354 Tg C yr-1 , which is considerably higher than the figure of 230 Tg C yr-1 in the current report1.This proof of concept demonstrates the relevance of complementing recent NFI data with remote sensing map products. Our study demonstrates that the already considerable value of forest inventory data can be further enhanced in a forest resources mapping scenario. In addition, we seek to promote greater access to these data by opening up their access to the larger scientific community. Through the integration of RS estimates of GSV and forest inventory data from Russia, we confirm that carbon stocks increased substantially during the last few decades in contrast to the figures provided in official national reporting. Russian forests play an even more important global role in carbon sequestration than previously thought, where the increase in growing stock is of the same magnitude as the net losses in tropical forests over the same time period. More

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    Ecological factors influence balancing selection on leaf chemical profiles of a wildflower

    1.Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics (Longman, 1996).2.Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).Article 

    Google Scholar 
    3.Kingsolver, J. G., Diamond, S. E., Siepielski, A. M. & Carlson, S. M. Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol. Ecol. 26, 1101–1118 (2012).Article 

    Google Scholar 
    4.Barrett, R. D. H. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38–44 (2008).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Kulbaba, M. W., Sheth, S. N., Pain, R. E., Eckhart, V. M. & Shaw, R. G. Additive genetic variance for lifetime fitness and the capacity for adaptation in an annual plant. Evolution 73, 1746–1758 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Lande, R. & Shannon, S. The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50, 434–437 (1996).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    7.Etterson, J. R. & Shaw, R. G. Constraint to adaptive evolution in response to global warming. Science 294, 151–154 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Anderson, J. T., Inouye, D. W., McKinney, A. M., Colautti, R. I. & Mitchell-Olds, T. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc. R. Soc. B 279, 3843–3852 (2012).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Steffen, W., Crutzen, P. J. & McNeil, J. R. The Anthropocene: are humans now overwhelming the great forces of nature? Ambio 36, 614–621 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    10.Zhang, X.-S. & Hill, W. G. Genetic variability under mutation selection balance. Trends Ecol. Evol. 20, 468–470 (2005).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.McGuigan, K., Aguirre, J. D. & Blows, M. W. Simultaneous estimation of additive and mutational genetic variance in an outbred population of Drosophila serrata. Genetics 201, 1239–1251 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Huang, W. et al. Spontaneous mutations and the origin and maintenance of quantitative genetic variation. eLife 5, e14625 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    13.Mitchell-Olds, T., Willis, J. H. & Goldstein, D. B. Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat. Rev. Genet. 8, 845–856 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Charlesworth, B. Causes of natural variation in fitness: evidence from studies of Drosophila populations. Proc. Natl Acad. Sci. USA 112, 1662–1669 (2015).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Subramaniam, B. & Rausher, M. D. Balancing selection on a floral polymorphism. Evolution 54, 691–695 (2000).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Charlesworth, D. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet. 2, e64 (2006).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    17.Hedrick, P. W. & Thomson, G. Evidence for balancing selection at HLA. Genetics 104, 449–456 (1983).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Troth, A., Puzey, J. R., Kim, R. S., Willis, J. H. & Kelly, J. K. Selective trade-offs maintain alleles underpinning complex trait variation in plants. Science 361, 475–478 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Delph, L. F. & Kelly, J. K. On the importance of balancing selection in plants. N. Phytol. 201, 45–56 (2014).Article 

    Google Scholar 
    20.Anderson, J. T., Wagner, M. R., Rushworth, C. A., Prasad, K. V. S. K. & Mitchell-Olds, T. The evolution of quantitative traits in complex environments. Heredity 112, 4–12 (2014).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Anderson, J. T. & Wadgymar, S. M. Climate change disrupts local adaptation and favours upslope migration. Ecol. Lett. 23, 181–192 (2020).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Agrawal, A. A. & Fishbein, M. Plant defense syndromes. Ecology 87, S132–S149 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Carmona, D., Lajeunesse, M. J. & Johnson, M. T. Plant traits that predict resistance to herbivores. Funct. Ecol. 25, 358–367 (2011).Article 

    Google Scholar 
    24.DeLucia, E. H., Nabity, P. D., Zavala, J. A. & Berenbaum, M. R. Climate change: resetting plant–insect interactions. Plant Physiol. 160, 1677–1685 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Mithöfer, A. & Boland, W. Plant defense against herbivores: chemical aspects. Annu. Rev. Plant Biol. 63, 431–450 (2012).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    26.Prasad, K. V. S. K. et al. A gain-of-function polymorphism controlling complex traits and fitness in nature. Science 337, 1081–1084 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Bergelson, J., Dwyer, G. & Emerson, J. J. Models and data on plant–enemy coevolution. Annu. Rev. Genet. 35, 469–499 (2001).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    28.Hodgins, K. A. & Barrett, S. C. H. Female reproductive success and the evolution of mating-type frequencies in tristylous populations. N. Phytol. 171, 569–580 (2006).Article 

    Google Scholar 
    29.Trotter, M. V. & Spencer, H. G. Complex dynamics occur in a single-locus, multiallelic model of general frequency-dependent selection. Theor. Popul. Biol. 76, 292–298 (2009).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Tuinstra, M. R., Ejeta, G. & Goldsbrough, P. B. Heterogeneous inbred family (HIF) analysis: a method for developing near-isogenic loci that differ at quantitative traits. Theor. Appl. Genet. 95, 1005–1011 (1997).CAS 
    Article 

    Google Scholar 
    31.Salehin, M. et al. Auxin-sensitive Aux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels. Nat. Commun. 10, 4021 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Hossain, M. S. et al. Glucosinolate degradation products, isothiocyanates, nitriles, and thiocyanates, induce stomatal closure accompanied by peroxidase-mediated reactive oxygen species production in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 77, 977–983 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Mitchell-Olds, T. & Schmitt, J. Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441, 947–952 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Wang, B. et al. Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta. Genome Biol. 20, 126 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Bloom, T. C., Baskin, J. M. & Baskin, C. C. Ecological life history of the facultative woodland biennial Arabis laevigata variety laevigata (Brassicaceae): seed dispersal. J. Torrey Bot. Soc. 129, 21–28 (2002).Article 

    Google Scholar 
    36.Song, B.-H. et al. Multilocus patterns of nucleotide diversity, population structure, and linkage disequilibrium in Boechera stricta, a wild relative of Arabidopsis. Genetics 181, 1021–1033 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Mackay, T., Stone, E. & Ayroles, J. The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10, 565–577 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    38.Hedrick, P. W. Genetic polymorphism in heterogeneous environments: a decade later. Annu. Rev. Ecol. Syst. 17, 535–566 (1986).Article 

    Google Scholar 
    39.Hedrick, P. W. Antagonistic pleiotropy and genetic polymorphism: a perspective. Heredity 82, 126–133 (1999).Article 

    Google Scholar 
    40.Turelli, M. & Barton, N. H. Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and G × E interactions. Genetics 166, 1053–1079 (2004).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Gillespie, J. H. & Langley, C. H. A general model to account for enzyme variation in natural populations. Genetics 76, 837–848 (1974).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Anderson, J. T., Willis, J. H. & Mitchell-Olds, T. Evolutionary genetics of plant adaptation. Trends Genet. 27, 258–266 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Anderson, J. T., Lee, C.-R., Rushworth, C. A., Colautti, R. I. & Mitchell-Olds, T. Genetic trade-offs and conditional neutrality contribute to local adaptation. Mol. Ecol. 22, 699–708 (2013).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Oakley, C. G., Ågren, J., Atchison, R. A. & Schemske, D. W. QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs. Mol. Ecol. 23, 4304–4315 (2014).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Price, N. et al. Combining population genomics and fitness QTLs to identify the genetics of local adaptation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 115, 5028–5033 (2018).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    46.Kettunen, J. et al. Genome-wide association study identifies multiple loci influencing human serum metabolite levels. Nat. Genet. 44, 269–276 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Abuelsoud, W., Hirschmann, F. & Papenbrock, J. in Drought Stress in Plants Vol. 1 (eds Hossain, M. A. et al.) 227–248 (Springer, 2016).48.Nguyen, D., Rieu, I., Mariani, C. & van Dam, N. M. How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Mol. Biol. 91, 727–740 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    49.Shani, E. M. et al. Plant stress tolerance requires auxin-sensitive Aux/IAA transcriptional repressors. Curr. Biol. 27, 437–444 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Hopkins, R. J., van Dam, N. M. & van Loon, J. J. A. Role of glucosinolates in insect–plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54, 57–83 (2009).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Burow, M., Müller, R., Gershenzon, J. & Wittstock, U. Altered glucosinolate hydrolysis in genetically engineered Arabidopsis thaliana and its influence on the larval development of Spodoptera littoralis. J. Chem. Ecol. 32, 2333–2349 (2006).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    52.Wagner, M. R. & Mitchell-Olds, T. Plasticity of plant defense and its evolutionary implications in wild populations of Boechera stricta. Evolution 72, 1034–1049 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Pagès, H., Aboyoun, P., Gentleman, R. & DebRoy, S. Biostrings: Efficient manipulation of biological strings. R package version 2.56.0 (2020).55.Wang et al. Correction to: Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta. Genome Biol. 20, 16 (2019).Article 

    Google Scholar 
    56.Carley, L. et al. Data to accompany: Ecological factors influence balancing selection on leaf chemical profiles of a wildflower. Dryad Data https://doi.org/10.5061/dryad.7h44j0zsr (2021).57.Atkinson, N. J., Lilley, C. J. & Urwin, P. E. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol. 162, 2028–2041 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Sharma, A. et al. Comprehensive analysis of plant rapid alkalization factor (RALF) genes. Plant Physiol. Biochem. 106, 82–90 (2016).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.Dutilleul, C., Jourdain, A., Bourguignon, J. & Hugouvieux, V. The Arabidopsis putative selenium-binding protein family: expression study and characterization of SBP1 as a potential new player in cadmium detoxification processes. Plant Physiol. 147, 239–251 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Jiang, S.-C. et al. Crucial roles of the pentatricopeptide repeat protein SOAR1 in Arabidopsis response to drought, salt and cold stresses. Plant Mol. Biol. 88, 369–385 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Wen, J., Vanek-Krebitz, M., Hoffmann-Sommergruber, K., Scheiner, O. & Breitender, H. The potential of Betv1 homologues, a nuclear multigene family, as phylogenetic markers in flowering plants. Mol. Phylogenet. Evol. 8, 317–333 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Koo, A. J., Fulda, M., Browse, J. & Ohlrogge, J. B. Identification of a plastid acyl‐acyl carrier protein synthetase in Arabidopsis and its role in the activation and elongation of exogenous fatty acids. Plant J. 44, 620–632 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Henrissat, B. et al. Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. Proc. Natl Acad. Sci. USA 92, 7090–7094 (1995).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar  More

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    Longevity and germination of Juniperus communis L. pollen after storage

    A uniform response of the pollen grains towards storage conditions was registered in all five shrubs investigated with a conspicuous decline in germination percentage and pollen tube length after storage. Pollen tube growth reacted more sensitively to storage than germination. The most profound reductions in pollen viability traits were observed in samples stored at + 4 °C. The germination percentage of freshly collected pollen of individual shrubs ranged between 67.3 and 88.6%, whereas that in stored pollen was between 18.0 and 39.6%. In relative terms, storage represented a 49.3–73.2% decline in germination (Fig. 1). The same tendency was also observed in pollen tube growth, when freshly collected pollen possessed 248.0–367.3 µm long pollen tubes, and pollen stored at + 4 °C was characterised by 93.9–218.5 µm long pollen tubes. The corresponding decline reached 32.5–68.7%.Figure 1Graphical illustrations of variation in pollen germination percentage (a) and pollen tube length (b) of individual shrubs revealed in fresh pollen and in pollen under storage. Different letters refer to the statistical significance of the differences between tested individuals and storage variants, resulting from Duncan’s pairwise tests.Full size imageContrary to storage at + 4 °C, pollen stored at − 20 °C had an increased germination by 0.3% in shrub no. 1 and 0.6% in shrub no. 5 as compared with fresh pollen. A more conspicuous increase in pollen germinability was registered in individual no. 4, exhibiting 70.0% germination in fresh pollen and 93.6% in pollen stored at − 20 °C. In the remaining two shrubs (no. 2, 3), only a negligible decline in pollen germination was recorded. The deviation from freshly collected pollen varied within 0.5–16.8%. In general, the germination characteristics of pollen stored at − 20 °C were comparable with those of the fresh pollen and varied between 67.6 and 93.6%. As a second viability trait, pollen tube growth deviated more profoundly from that of fresh pollen than germination. On average, the pollen tube length of pollen stored at − 20 °C ranged from 163.0 to 286.6 µm, which represents a 11.4–45.7% decline compared to fresh pollen (Figs. 1, S1). ANOVA and Duncan`s grouping confirmed the highly significant differences between tested shrubs in both pollen germination percentage (P  More

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    Helarchaeota and co-occurring sulfate-reducing bacteria in subseafloor sediments from the Costa Rica Margin

    1.Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D’Hondt S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci USA. 2012;109:16213–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Lloyd KG, May MK, Kevorkian RT, Steen AD. Meta-analysis of quantification methods shows that Archaea and Bacteria have similar abundances in the subseafloor. Appl Environ Microbiol. 2013;79:7790–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Hoshino T, Inagaki F. Abundance and distribution of Archaea in the subseafloor sedimentary biosphere. ISME J. 2019;13:227–31.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    4.Lipp JS, Morono Y, Inagaki F, Hinrichs K-U. Significant contribution of Archaea to extant biomass in marine subsurface sediments. Nature. 2008;454:991–4.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Vuillemin A, Wankel SD, Coskun ÖK, Magritsch T, Vargas S, Estes ER, et al. Archaea dominate oxic subseafloor communities over multimillion-year time scales. Sci Adv. 2019;5:eaaw4108.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Zhao R, Hannisdal B, Mogollon JM, Jørgensen SL. Nitrifier abundance and diversity peak at deep redox transition zones. Sci Rep. 2019;9:8633.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    7.Hiraoka S, Hirai M, Matsui Y, Makabe A, Minegishi H, Tsuda M, et al. Microbial community and geochemical analyses of trans-trench sediments for understanding the roles of hadal environments. ISME J. 2020;14:740–56.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    8.Hoshino T, Doi H, Uramoto GI, Wörmer L, Adhikari RR, Xiao N, et al. Global diversity of microbial communities in marine sediment. Proc Natl Acad Sci. 2020;117:27587–97.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    9.Durbin AM, Teske A. Archaea in organic-lean and organic-rich marine subsurface sediments: an environmental gradient reflected in distinct phylogenetic lineages. Front Microbiol. 2012;3:168.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    10.Biddle JF, Lipp JS, Lever MA, Lloyd KG, Sørensen KB, Anderson R, et al. Heterotrophic archaea dominate sedimentary subsurface ecosystems off Peru. Proc Natl Acad Sci USA. 2006;103:3846–51.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    11.Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, et al. Predominant archaea in marine sediments degrade detrital proteins. Nature. 2013;496:215–8.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Yu T, Wu W, Liang W, Lever MA, Hinrichs K-U, Wang F. Growth of sedimentary Bathyarchaeota on lignin as an energy source. Proc Natl Acad Sci. 2018;115:6022–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Zaremba-Niedzwiedzka K, Caceres EF, Saw JH, Bäckström D, Juzokaite L, Vancaester E, et al. Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature. 2017;541:353–8.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature. 2015;521:173–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Spang A, Caceres EF, Ettema TJG. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science. 2017;357:eaaf3883.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    16.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–D596.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    17.Manoharan L, Kozlowski JA, Murdoch RW, Löffler FE, Sousa FL, Schleper C. Metagenomes from coastal marine sediments give insights into the ecological role and cellular features of Loki-and Thorarchaeota. mBio. 2019;10:e02039–02019.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    18.Imachi H, Nobu MK, Nakahara N, Morono Y, Ogawara M, Takaki Y, et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature. 2020;577:519–25.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Seitz KW, Dombrowski N, Eme L, Spang A, Lombard J, Sieber JR, et al. Asgard archaea capable of anaerobic hydrocarbon cycling. Nat Commun. 2019;10:1822.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    20.Farag IF, Zhao R, Biddle JF. “Sifarchaeota” a novel Asgard phylum from Costa Rican sediment capable of polysaccharide degradation and anaerobic methylotrophy. Appl Environ Microbiol. 2021;87:e02584–02520.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Spang A, Stairs CW, Dombrowski N, Eme L, Lombard J, Caceres EF, et al. Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nat Microbiol. 2019;4:1138–48.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Laso-Pérez R, Wegener G, Knittel K, Widdel F, Harding KJ, Krukenberg V, et al. Thermophilic archaea activate butane via alkyl-coenzyme M formation. Nature. 2016;539:396–401.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    23.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 
    24.Wang Y, Wegener G, Hou J, Wang F, Xiao X. Expanding anaerobic alkane metabolism in the domain of Archaea. Nat Microbiol. 2019;4:595–602.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Laso-Pérez R, Hahn C, van Vliet DM, Tegetmeyer HE, Schubotz F, Smit NT, et al. Anaerobic degradation of non-methane alkanes by “Candidatus Methanoliparia” in hydrocarbon seeps of the Gulf of Mexico. mBio. 2019;10:e01814–01819.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Krukenberg V, Harding K, Richter M, Glöckner FO, Gruber-Vodicka HR, Adam B, et al. Candidatus Desulfofervidus auxilii, a hydrogenotrophic sulfate‐reducing bacterium involved in the thermophilic anaerobic oxidation of methane. Environ Microbiol. 2016;18:3073–91.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Martino A, Rhodes ME, León-Zayas R, Valente IE, Biddle JF, House CH. Microbial diversity in sub-seafloor sediments from the Costa Rica Margin. Geosciences. 2019;9:218.CAS 
    Article 

    Google Scholar 
    28.Farag IF, Biddle JF, Zhao R, Martino AJ, House CH, León-Zayas RI. Metabolic potentials of archaeal lineages resolved from metagenomes of deep Costa Rica sediments. ISME J. 2020;14:1345–58.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Barry PH, de Moor JM, Giovannelli D, Schrenk M, Hummer DR, Lopez T, et al. Forearc carbon sink reduces long-term volatile recycling into the mantle. Nature. 2019;568:487–92.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Expedition 334 Scientists. Site U1379. In Vannucchi, P, Ujiie, K, Stroncik, N, Malinverno, A, and the Expedition 334 Scientists, Proc IODP, 334: Tokyo (Integrated Ocean Drilling Program Management International, Inc) (2012).31.Formolo M, Nuzzo M, Torres M, Solomon E. Expedition I Gas geochemical results from IODP Expedition 334: Influence of subsurface structure and fluid flow on gas composition. In: Proceedings of AGU Fall Meeting Abstracts) 2011.32.Boyd JA, Woodcroft BJ, Tyson GW. GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes. Nucleic Acids Res. 2018;46:e59.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    33.Singleton CM, McCalley CK, Woodcroft BJ, Boyd JA, Evans PN, Hodgkins SB, et al. Methanotrophy across a natural permafrost thaw environment. ISME J. 2018;12:2544–58.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Borrel G, Adam PS, McKay LJ, Chen LX, Sierra-García IN, Sieber C, et al. Wide diversity of methane and short-chain alkane metabolisms in uncultured archaea. Nat Microbiol. 2019;4:603–13.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Hua Z-S, Wang YL, Evans PN, Qu YN, Goh KM, Rao YZ, et al. Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea. Nat Commun. 2019;10:1–11.Article 
    CAS 

    Google Scholar 
    36.Cai M, et al. Diverse Asgard archaea including the novel phylum Gerdarchaeota participate in organic matter degradation. Science China Life Sciences, (2020).37.Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11:2399–406.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Hahn CJ, Laso-Pérez R, Vulcano F, Vaziourakis KM, Stokke R, Steen IH, et al. “Candidatus Ethanoperedens,” a thermophilic genus of Archaea mediating the anaerobic oxidation of ethane. mBio. 2020;11:e00600–00620.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Rastogi S, Liberles DA. Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evolut Biol. 2005;5:28.Article 
    CAS 

    Google Scholar 
    40.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 
    41.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 
    42.Skennerton CT, Chourey K, Iyer R, Hettich RL, Tyson GW, Orphan VJ. Methane-fueled syntrophy through extracellular electron transfer: uncovering the genomic traits conserved within diverse bacterial partners of anaerobic methanotrophic archaea. mBio. 2017;8:e00530–00517.PubMed 
    PubMed Central 

    Google Scholar 
    43.Beulig F, Røy H, McGlynn SE, Jørgensen BB. Cryptic CH4 cycling in the sulfate–methane transition of marine sediments apparently mediated by ANME-1 archaea. ISME J. 2019;13:250–62.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    45.Dombrowski N, Teske AP, Baker BJ. Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments. Nat Commun. 2018;9:4999.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    46.Dong X, Greening C, Rattray JE, Chakraborty A, Chuvochina M, Mayumi D, et al. Metabolic potential of uncultured bacteria and archaea associated with petroleum seepage in deep-sea sediments. Nat Commun. 2019;10:1816.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    47.Brown CT, Olm MR, Thomas BC, Banfield JF. Measurement of bacterial replication rates in microbial communities. Nat Biotechnol. 2016;34:1256–63.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    48.Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J. 2016;10:761–77.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    49.Shimoyama T, Kato S, Ishii SI, Watanabe K. Flagellum mediates symbiosis. Science. 2009;323:1574–1574.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    50.Valentine DL, Reeburgh WS. New perspectives on anaerobic methane oxidation: minireview. Environ Microbiol. 2000;2:477–84.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    51.Vannucchi P, Ujiie K, Stroncik N, the IESP. IODP Expedition 334: An investigation of the sedimentary record, fluid flow and state of stress on top of the seismogenic zone of an erosive subduction margin. Sci Dril. 2013;15:23–30.Article 

    Google Scholar 
    52.Torres ME, Muratli JM, Solomon EA Data report: minor element concentrations in pore fluids from the CRISP-A transect drilled during Expedition 334. In: Proceeding sof IODP | Volume) 2014.53.Riedinger N, Torres ME, Screaton E, Solomon EA, Kutterolf S, Schindlbeck‐Belo J, et al. Interplay of subduction tectonics, sedimentation, and carbon cycling. Geochem, Geophys, Geosyst. 2019;20:4939–55.CAS 
    Article 

    Google Scholar 
    54.Andrews S. FastQC: a quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ 2010.55.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 
    56.Gruber-Vodicka HR, Seah BKB, Pruesse E. phyloFlash: rapid small-subunit rRNA profiling and targeted assembly from metagenomes. mSystems. 2020;5:e00920–00920.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    57.Li DH, Liu CM, Luo RB, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    58.Wu YW, Simmons BA, Singer SW. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2016;32:605–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    59.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 
    60.Seah BK, Gruber-Vodicka HR. gbtools: interactive visualization of metagenome bins in R. Front. Microbiol. 2015;6:1451.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Bushnell B. BBMap: a fast, accurate, splice-aware aligner. Ernest Orlando Lawrence Berkeley National Laboratory, Berkeley, CA (US) (2014).62.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 
    63.Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.CAS 
    Article 

    Google Scholar 
    64.Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2016;44:D286–D293.CAS 
    Article 

    Google Scholar 
    65.Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428:726–31.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    66.Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research. 2011;40:D109–D114.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    67.Garcia PS, Jauffrit F, Grangeasse C. Brochier-Armanet C. GeneSpy, a user-friendly and flexible genomic context visualizer. Bioinformatics. 2018;35:329–31.Article 
    CAS 

    Google Scholar 
    68.Badalamenti JP, Summers ZM, Chan CH, Gralnick JA, Bond DR. Isolation and genomic characterization of ‘Desulfuromonas soudanensis WTL’, a metal-and electrode-respiring bacterium from anoxic deep subsurface brine. Front Microbiol. 2016;7:913.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    69.Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.Article 
    CAS 

    Google Scholar 
    70.Hernsdorf AW, Amano Y, Miyakawa K, Ise K, Suzuki Y, Anantharaman K, et al. Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments. ISME J. 2017;11:1915–29.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9:5114.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    72.Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Sorek R, Zhu YW, Creevey CJ, Francino MP, Bork P, Rubin EM. Genome-wide experimental determination of barriers to horizontal gene transfer. Science. 2007;318:1449–52.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    74.Campbell JH, O’Donoghue P, Campbell AG, Schwientek P, Sczyrba A, Woyke T, et al. UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota. Proc Natl Acad Sci USA. 2013;110:5540–5.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    75.Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, et al. Anvi’o: an advanced analysis and visualization platformfor ‘omics data. PeerJ. 2015;3:e1319.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.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 
    77.Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evolut. 2015;32:268–74.CAS 
    Article 

    Google Scholar 
    79.Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    80.Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evolut. 2018;35:518–22.CAS 
    Article 

    Google Scholar 
    81.Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evolut. 2013;30:772–80.CAS 
    Article 

    Google Scholar 
    83.Okonechnikov K, Golosova O, Fursov M, Team U. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics. 2012;28:1166–7.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Matheus Carnevali PB, Schulz F, Castelle CJ, Kantor RS, Shih PM, Sharon I, et al. Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria. Nat Commun. 2019;10:463.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    85.Kessler AJ, Chen YJ, Waite DW, Hutchinson T, Koh S, Popa ME, et al. Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments. Nat Microbiol. 2019;4:1014–23.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    86.R Development Core Team. R: a language and environment for statistical computing.). R foundation for statistical computing, Vienna, Austria (2011). More

  • in

    Changes in soil microbial community and activity caused by application of dimethachlor and linuron

    1.Food and Agriculture Organization of the United Nations. FAOSTAT Database., http://www.fao.org/faostat/en/#home (2020).2.Sharma, A. et al. Worldwide pesticide usage and its impacts on ecosystem. SN Appl. Sci. 1, 1446. https://doi.org/10.1007/s42452-019-1485-1 (2019).CAS 
    Article 

    Google Scholar 
    3.Peterson, M. A., Collavo, A., Ovejero, R., Shivrain, V. & Walsh, M. J. The challenge of herbicide resistance around the world: A current summary. Pest. Manag. Sci. 74, 2246–2259. https://doi.org/10.1002/ps.4821 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    4.Landrigan, P. J. & Benbrook, C. GMOs, herbicides, and public health. N. Engl. J. Med. 373, 693–695 (2015).Article 

    Google Scholar 
    5.Horwath, W. R. The role of the soil microbial biomass in cycling nutrients. Microbial biomass: A paradigm shift in terrestrial biogeochemistry. World Sci. 41–66 https://doi.org/10.1142/9781786341310_0002 (2017).6.Meena, R. S. et al. Impact of agrochemicals on soil microbiota and management: A review. Land 9, 34 (2020).Article 

    Google Scholar 
    7.Perucci, P., Vischetti, C. & Battistoni, F. Rimsulfuron in a silty clay loam soil: Effects upon microbiological and biochemical properties under varying microcosm conditions. Soil Biol. Biochem. 31, 195–204 (1999).Article 

    Google Scholar 
    8.Huang, X. et al. Microbial catabolism of chemical herbicides: Microbial resources, metabolic pathways and catabolic genes. Pestic. Biochem. Physiol. 143, 272–297 (2017).CAS 
    Article 

    Google Scholar 
    9.Lewis, K. A., Tzilivakis, J., Warner, D. J. & Green, A. An international database for pesticide risk assessments and management. Hum. Ecol. Risk Assess. 22, 1050–1064. https://doi.org/10.1080/10807039.2015.1133242 (2016).CAS 
    Article 

    Google Scholar 
    10.Syngenta. Teridox label, https://www.syngenta.sk/sites/g/files/zhg356/f/etiketa_teridox_500_ec.pdf (2014).11.European Food Safety Authority. Conclusion regarding the peer review of the pesticide risk assessment of the active substance dimethachlor. EFSA J. 6, 169r (2008).
    Google Scholar 
    12.López-Ruiz, R., Romero-González, R., Ortega-Carrasco, E., Martínez Vidal, J. L. & Garrido Frenich, A. Degradation studies of dimethachlor in soils and water by UHPLC-HRMS: Putative elucidation of unknown metabolites. Pest. Manag. Sci. 76, 721–729. https://doi.org/10.1002/ps.5570 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Rasmussen, J., Aamand, J., Rosenberg, P., Jacobsen, O. S. & Sørensen, S. R. Spatial variability in the mineralisation of the phenylurea herbicide linuron within a Danish agricultural field: Multivariate correlation to simple soil parameters. Pest Manag. Sci. Formerly Pesticide Sci. 61, 829–837 (2005).CAS 
    Article 

    Google Scholar 
    14.European Food Safety Authority. Peer review of the pesticide risk assessment of the active substance linuron. EFSA J. 14, e04518 (2016).
    Google Scholar 
    15.Crouzet, O. et al. Response of soil microbial communities to the herbicide mesotrione: A dose-effect microcosm approach. Soil Biol. Biochem. 42, 193–202. https://doi.org/10.1016/j.soilbio.2009.10.016 (2010).CAS 
    Article 

    Google Scholar 
    16.Latkovic, D. et al. Case study upon foliar application of biofertilizers affecting microbial biomass and enzyme activity in soil and yield related prop. Biology 9, 452 (2020).CAS 
    Article 

    Google Scholar 
    17.Nannipieri, P. et al. Beyond microbial diversity for predicting soil functions: A mini review. Pedosphere 30, 5–17. https://doi.org/10.1016/S1002-0160(19)60824-6 (2020).Article 

    Google Scholar 
    18.Krogh, K. A., Halling-Sørensen, B., Mogensen, B. B. & Vejrup, K. V. Environmental properties and effects of nonionic surfactant adjuvants in pesticides: A review. Chemosphere 50, 871–901. https://doi.org/10.1016/S0045-6535(02)00648-3 (2003).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    19.García-Ortega, S., Holliman, P. J. & Jones, D. L. Toxicology and fate of Pestanal® and commercial propetamphos formulations in river and estuarine sediment. Sci. Total Environ. 366, 826–836. https://doi.org/10.1016/j.scitotenv.2005.08.008 (2006).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    20.Medo, J., Maková, J., Kovácsová, S., Majerčíková, K. & Javoreková, S. Effect of Dursban 480 EC (chlorpyrifos) and Talstar 10 EC (bifenthrin) on the physiological and genetic diversity of microorganisms in soil. J. Environ. Sci. Health B 50, 871–883 (2015).CAS 
    Article 

    Google Scholar 
    21.Cycoń, M., Piotrowska-Seget, Z. & Kozdrój, J. Dehydrogenase activity as an indicator of different microbial responses to pesticide-treated soils. Chem. Ecol. 26, 243–250. https://doi.org/10.1080/02757540.2010.495062 (2010).CAS 
    Article 

    Google Scholar 
    22.Singh, M. K., Singh, N. K. & Singh, S. P. In Plant Responses to Soil Pollution (eds Singh, P. et al.) 179–194 (Springer Singapore, 2020). https://doi.org/10.1007/978-981-15-4964-9_11Chapter 

    Google Scholar 
    23.Makova, J., Javorekova, S., Medo, J. & Majerčíková, K. Characteristics of microbial biomass carbon and respiration activities in arable soil and pasture grassland soil. J. Cent. Eur. Agric. 12, 0–0 (2011).Article 

    Google Scholar 
    24.Imfeld, G. & Vuilleumier, S. Measuring the effects of pesticides on bacterial communities in soil: A critical review. Eur. J. Soil Biol. 49, 22–30. https://doi.org/10.1016/j.ejsobi.2011.11.010 (2012).CAS 
    Article 

    Google Scholar 
    25.Nguyen, D. B., Rose, M. T., Rose, T. J., Morris, S. G. & van Zwieten, L. Impact of glyphosate on soil microbial biomass and respiration: A meta-analysis. Soil Biol. Biochem. 92, 50–57. https://doi.org/10.1016/j.soilbio.2015.09.014 (2016).CAS 
    Article 

    Google Scholar 
    26.Mesnage, R. & Antoniou, M. N. Ignoring adjuvant toxicity falsifies the safety profile of commercial pesticides. Front Public Health https://doi.org/10.3389/fpubh.2017.00361 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    27.Haney, R., Senseman, S., Krutz, L. & Hons, F. Soil carbon and nitrogen mineralization as affected by atrazine and glyphosate. Biol. Fertil. Soils 35, 35–40. https://doi.org/10.1007/s00374-001-0437-1 (2002).CAS 
    Article 

    Google Scholar 
    28.Ratcliff, A. W., Busse, M. D. & Shestak, C. J. Changes in microbial community structure following herbicide (glyphosate) additions to forest soils. Appl. Soil Ecol. 34, 114–124. https://doi.org/10.1016/j.apsoil.2006.03.002 (2006).Article 

    Google Scholar 
    29.Sofo, A., Scopa, A., Dumontet, S., Mazzatura, A. & Pasquale, V. Toxic effects of four sulphonylureas herbicides on soil microbial biomass. J. Environ. Sci. Health B 47, 653–659. https://doi.org/10.1080/03601234.2012.669205 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    30.Lee, S.-H., Kim, M.-S., Kim, J.-G. & Kim, S.-O. Use of soil enzymes as indicators for contaminated soil monitoring and sustainable management. Sustainability 12, 8209 (2020).CAS 
    Article 

    Google Scholar 
    31.Wolińska, A. & Stępniewska, Z. Dehydrogenase activity in the soil environment. Dehydrogenases 10, 183–210 (2012).
    Google Scholar 
    32.Pozo, C., Salmeron, V., Rodelas, B., Martinez-Toledo, M. V. & Gonzalez-Lopez, J. Effects of the herbicide alachlor on soil microbial activities. Ecotoxicology 3, 4–10. https://doi.org/10.1007/BF00121384 (1994).CAS 
    Article 
    PubMed 

    Google Scholar 
    33.Sebiomo, A., Ogundero, V. & Bankole, S. Effect of four herbicides on microbial population, soil organic matter and dehydrogenase activity. Afr. J. Biotechnol. 10, 770–778 (2011).CAS 

    Google Scholar 
    34.Pertile, M. et al. Responses of soil microbial biomass and enzyme activity to herbicides imazethapyr and flumioxazin. Sci. Rep. 10, 7694. https://doi.org/10.1038/s41598-020-64648-3 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Dzionek, A., Dzik, J., Wojcieszyńska, D. & Guzik, U. Fluorescein diacetate hydrolysis using the whole biofilm as a sensitive tool to evaluate the physiological state of immobilized bacterial cells. Catalysts 8, 434 (2018).Article 

    Google Scholar 
    36.Das, P., Pal, R. & Chowdhury, A. Effect of novaluron on microbial biomass, respiration, and fluorescein diacetate-hydrolyzing activity in tropical soils. Biol. Fertil. Soils 44, 387–391. https://doi.org/10.1007/s00374-007-0219-5 (2007).Article 

    Google Scholar 
    37.Zabaloy, M. C., Garland, J. L. & Gómez, M. A. An integrated approach to evaluate the impacts of the herbicides glyphosate, 2,4-D and metsulfuron-methyl on soil microbial communities in the Pampas region, Argentina. Appl. Soil. Ecol. 40, 1–12. https://doi.org/10.1016/j.apsoil.2008.02.004 (2008).Article 

    Google Scholar 
    38.Perucci, P., Dumontet, S., Bufo, S. A., Mazzatura, A. & Casucci, C. Effects of organic amendment and herbicide treatment on soil microbial biomass. Biol. Fertil. Soils 32, 17–23. https://doi.org/10.1007/s003740000207 (2000).CAS 
    Article 

    Google Scholar 
    39.Medo, J. et al. Effects of sulfonylurea herbicides chlorsulfuron and sulfosulfuron on enzymatic activities and microbial communities in two agricultural soils. Environ. Sci. Pollut. Res. 27, 41265–41278 (2020).CAS 
    Article 

    Google Scholar 
    40.Dennis, P. G., Kukulies, T., Forstner, C., Orton, T. G. & Pattison, A. B. The effects of glyphosate, glufosinate, paraquat and paraquat-diquat on soil microbial activity and bacterial, archaeal and nematode diversity. Sci. Rep. 8, 2119 (2018).ADS 
    Article 

    Google Scholar 
    41.Du, P. et al. Clomazone influence soil microbial community and soil nitrogen cycling. Sci. Total Environ. 644, 475–485. https://doi.org/10.1016/j.scitotenv.2018.06.214 (2018).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    42.Elsayed, O. F., Maillard, E., Vuilleumier, S., Millet, M. & Imfeld, G. Degradation of chloroacetanilide herbicides and bacterial community composition in lab-scale wetlands. Sci. Total Environ. 520, 222–231. https://doi.org/10.1016/j.scitotenv.2015.03.061 (2015).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    43.Chauhan, A., Pathak, A., Ewida, A. Y., Griffiths, Z. & Stothard, P. Whole genome sequence analysis of an Alachlor and Endosulfan degrading Pseudomonas strain W15Feb9B isolated from Ochlockonee River, Florida. Genom. Data 8, 134–138 (2016).Article 

    Google Scholar 
    44.Xu, C., Ding, J., Qiu, J. & Ma, Y. Biodegradation of acetochlor by a newly isolated Achromobacter sp. strain D-12. J. Environ. Sci. Health B 48, 960–966. https://doi.org/10.1080/03601234.2013.816601 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    45.Dwivedi, S., Singh, B., Al-Khedhairy, A., Alarifi, S. & Musarrat, J. Isolation and characterization of butachlor-catabolizing bacterial strain Stenotrophomonas acidaminiphila JS-1 from soil and assessment of its biodegradation potential. Lett. Appl. Microbiol. 51, 54–60 (2010).CAS 
    PubMed 

    Google Scholar 
    46.Mohanty, S. S. & Jena, H. M. Degradation kinetics and mechanistic study on herbicide bioremediation using hyper butachlor-tolerant Pseudomonas putida G3. Process Saf. Environ. Prot. 125, 172–181 (2019).CAS 
    Article 

    Google Scholar 
    47.Öztürk, B. et al. Comparative genomics suggests mechanisms of genetic adaptation towards the catabolism of the phenylurea herbicide linuron in Variovorax. Genome Biol. Evol. https://doi.org/10.1093/gbe/evaa085 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    48.Sørensen, S. R., Ronen, Z. & Aamand, J. Isolation from agricultural soil and characterization of a Sphingomonas sp. able to mineralize the phenylurea herbicide isoproturon. Appl. Environ. Microbiol. 67, 5403–5409 (2001).Article 

    Google Scholar 
    49.Batisson, I., Pesce, S., Besse-Hoggan, P., Sancelme, M. & Bohatier, J. Isolation and characterization of diuron-degrading bacteria from lotic surface water. Microb. Ecol. 54, 761–770 (2007).CAS 
    Article 

    Google Scholar 
    50.Villaverde, J., Rubio-Bellido, M., Merchán, F. & Morillo, E. Bioremediation of diuron contaminated soils by a novel degrading microbial consortium. J. Environ. Manag. 188, 379–386 (2017).CAS 
    Article 

    Google Scholar 
    51.Cassel, D. & Nielsen, D. Field capacity and available water capacity. Methods Soil Anal. Part 1 Phys. Mineral. Methods 5, 901–926 (1986).
    Google Scholar 
    52.Alef, K. Soil respiration. In Methods in Applied Soil Microbiology and Biochemistry (eds Alef, P. & Nannipieri, K.) 214–218 (Academic Press, 1995).
    Google Scholar 
    53.Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41, e1–e1 (2013).CAS 
    Article 

    Google Scholar 
    54.Fadrosh, D. W. et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014).Article 

    Google Scholar 
    55.Vetrovský, T., Baldrian, P., Morais, D. & Berger, B. SEED 2: A user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics 1, 3 (2018).
    Google Scholar 
    56.Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852–857 (2019).CAS 
    Article 

    Google Scholar 
    57.Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
    Article 

    Google Scholar 
    58.Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).CAS 
    Article 

    Google Scholar 
    59.Douglas, G. M. et al. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 1–5 https://doi.org/10.1038/s41587-020-0548-6 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    60.Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 1–21 (2014).Article 

    Google Scholar 
    61.Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J. & Knight, R. UniFrac: An effective distance metric for microbial community comparison. ISME J 5, 169–172 (2011).Article 

    Google Scholar 
    62.Vance, E. D., Brookes, P. C. & Jenkinson, D. S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703–707 (1987).CAS 
    Article 

    Google Scholar 
    63.Casida, L. Jr., Klein, D. & Santoro, T. Soil dehydrogenase activity. Soil Sci. 98, 371–376 (1964).ADS 
    CAS 
    Article 

    Google Scholar 
    64.Green, V. S., Stott, D. E. & Diack, M. Assay for fluorescein diacetate hydrolytic activity: Optimization for soil samples. Soil Biol. Biochem. 38, 693–701. https://doi.org/10.1016/j.soilbio.2005.06.020 (2006).CAS 
    Article 

    Google Scholar 
    65.R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).66.Oksanen, J. et al. Package ‘vegan’. Community ecology package, version 2 (2013). More