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    Potential metabolic and genetic interaction among viruses, methanogen and methanotrophic archaea, and their syntrophic partners

    Evans PN, Boyd JA, Leu AO, Woodcroft BJ, Parks DH, Hugenholtz P, et al. An evolving view of methane metabolism in the Archaea. Nat Rev Microbiol. 2019;17:219–32.CAS 
    PubMed 

    Google Scholar 
    Reeburgh WS. Oceanic methane biogeochemistry. Chem Rev. 2007;107:486–513.CAS 
    PubMed 

    Google Scholar 
    Timmers PHA, Welte CU, Koehorst JJ, Plugge CM, Jetten MSM, Stams AJM. Reverse methanogenesis and respiration in methanotrophic Archaea. Archaea. 2017;2017:1–22.
    Google Scholar 
    Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, Richardson PM, et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science. 2004;305:1457–62.CAS 
    PubMed 

    Google Scholar 
    Knittel K, Boetius A. Anaerobic oxidation of methane: progress with an unknown process. Annu Rev Microbiol. 2009;63:311–34.CAS 
    PubMed 

    Google Scholar 
    Vanwonterghem I, Evans PN, Parks DH, Jensen PD, Woodcroft BJ, Hugenholtz P, et al. Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat Microbiol. 2016;1:16170.CAS 
    PubMed 

    Google Scholar 
    McKay LJ, Dlakić M, Fields MW, Delmont TO, Eren AM, Jay ZJ, et al. Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota. Nat Microbiol. 2019;4:614–22.CAS 
    PubMed 

    Google Scholar 
    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 

    Google Scholar 
    Wang Y, Wegener G, Ruff SE, Wang F. Methyl/alkyl‐coenzyme M reductase‐based anaerobic alkane oxidation in archaea. Environ Microbiol. 2021;23:530–41.CAS 
    PubMed 

    Google Scholar 
    Bertram S, Blumenberg M, Michaelis W, Siegert M, Krüger M, Seifert R. Methanogenic capabilities of ANME‐archaea deduced from 13C‐labelling approaches. Environ Microbiol. 2013;15:2384–93.CAS 
    PubMed 

    Google Scholar 
    Sousa DZ, Smidt H, Alves MM, Stams AJM. Syntrophomonas zehnderi sp. nov., an anaerobe that degrades long-chain fatty acids in co-culture with Methanobacterium formicicum. Int J Syst Evol Micr. 2007;57:609–15.CAS 

    Google Scholar 
    Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, Harada H, et al. Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evol Micr. 2006;56:1331–40.CAS 

    Google Scholar 
    Yamada T, Sekiguchi Y, Imachi H, Kamagata Y, Ohashi A, Harada H. Diversity, localization, and physiological properties of filamentous microbes belonging to Chloroflexi subphylum I in mesophilic and thermophilic methanogenic sludge granules. Appl Environ Microb. 2005;71:7493–503.CAS 

    Google Scholar 
    Manzoor S, Schnürer A, Bongcam-Rudloff E, Müller B. Complete genome sequence of Methanoculleus bourgensis strain MAB1, the syntrophic partner of mesophilic acetate-oxidising bacteria (SAOB). Stand Genomic Sci. 2016;11:80.PubMed 
    PubMed Central 

    Google Scholar 
    Engelhardt T, Sahlberg M, Cypionka H, Engelen B. Biogeography of Rhizobium radiobacter and distribution of associated temperate phages in deep subseafloor sediments. ISME J. 2013;7:199–209.CAS 
    PubMed 

    Google Scholar 
    Nölling J, Groffen A, de Vos WM. φ F1 and φF3, two novel virulent, archaeal phages infecting different thermophilic strains of the genus. Methanobacterium Microbiol. 1993;139:2511–6.
    Google Scholar 
    Meile L, Jenal U, Studer D, Jordan M, Leisinger T. Characterization of ψM1, a virulent phage of Methanobacterium thermoautotrophicum Marburg. Arch Microbiol. 1989;152:105–10.CAS 

    Google Scholar 
    Weidenbach K, Nickel L, Neve H, Alkhnbashi OS, Künzel S, Kupczok A, et al. Methanosarcina spherical virus, a novel archaeal lytic virus targeting Methanosarcina strains. J Virol. 2017;91:e00955–17.PubMed 
    PubMed Central 

    Google Scholar 
    Molnár J, Magyar B, Schneider G, Laczi K, Valappil SK, Kovács ÁL, et al. Identification of a novel archaea virus, detected in hydrocarbon polluted Hungarian and Canadian samples. PLOS ONE. 2020;15:e0231864.PubMed 
    PubMed Central 

    Google Scholar 
    Paul BG, Bagby SC, Czornyj E, Arambula D, Handa S, Sczyrba A, et al. Targeted diversity generation by intraterrestrial archaea and archaeal viruses. Nat Commun. 2015;6:6585.CAS 
    PubMed 

    Google Scholar 
    Pourcel C, Touchon M, Villeriot N, Vernadet J-P, Couvin D, Toffano-Nioche C, et al. CRISPRCasdb a successor of CRISPRdb containing CRISPR arrays and cas genes from complete genome sequences, and tools to download and query lists of repeats and spacers. Nucleic Acids Res. 2019;48:D535–D544.PubMed Central 

    Google Scholar 
    Roux S, Hallam SJ, Woyke T, Sullivan MB. Viral dark matter and virus–host interactions resolved from publicly available microbial genomes. eLife. 2015;4:e08490.PubMed Central 

    Google Scholar 
    Lever MA, Teske AP. Diversity of methane-cycling Archaea in hydrothermal sediment investigated by general and group-specific PCR primers. Appl Environ Microb. 2015;81:1426–41.
    Google Scholar 
    Jian H, Yi Y, Wang J, Hao Y, Zhang M, Wang S, et al. Diversity and distribution of viruses inhabiting the deepest ocean on Earth. ISME J. 2021;15:3094–110.Paez-Espino D, Pavlopoulos GA, Ivanova NN, Kyrpides NC. Nontargeted virus sequence discovery pipeline and virus clustering for metagenomic data. Nature Protoc. 2017;12:1673–82.CAS 

    Google Scholar 
    Roux S, Enault F, Hurwitz BL, Sullivan MB. VirSorter: mining viral signal from microbial genomic data. PeerJ. 2015;3:e985.PubMed 
    PubMed Central 

    Google Scholar 
    Ren J, Song K, Deng C, Ahlgren NA, Fuhrman JA, Li Y, et al. Identifying viruses from metagenomic data using deep learning. Quant Biol. 2020;8:64–77.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Roux S, Páez-Espino D, Chen I-MA, Palaniappan K, Ratner A, Chu K, et al. IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses. Nucleic Acids Res. 2020;49:D764–D775.PubMed Central 

    Google Scholar 
    Nayfach S, Camargo AP, Schulz F, Eloe-Fadrosh E, Roux S, Kyrpides NC. CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nat Biotechnol. 2021;39:578–85.CAS 
    PubMed 

    Google Scholar 
    Sandaa R, Gómez‐Consarnau L, Pinhassi J, Riemann L, Malits A, Weinbauer MG, et al. Viral control of bacterial biodiversity – evidence from a nutrient‐enriched marine mesocosm experiment. Environ Microbiol. 2009;11:2585–97.CAS 
    PubMed 

    Google Scholar 
    Howard-Varona C, Hargreaves KR, Abedon ST, Sullivan MB. Lysogeny in nature: mechanisms, impact and ecology of temperate phages. ISME J. 2017;11:1511–20.PubMed 
    PubMed Central 

    Google Scholar 
    Li Z, Pan D, Wei G, Pi W, Zhang C, Wang J-H, et al. Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity. ISME J. 2021;15:2366–78.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Krupovič M, Forterre P, Bamford DH. Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria. J Mol Biol. 2010;397:144–60.PubMed 

    Google Scholar 
    Thiroux S, Dupont S, Nesbø CL, Bienvenu N, Krupovic M, L’Haridon S, et al. The first head‐tailed virus, MFTV1, infecting hyperthermophilic methanogenic deep‐sea archaea. Environ Microbiol. 2021;23:3614–26.CAS 
    PubMed 

    Google Scholar 
    Jang HB, Bolduc B, Zablocki O, Kuhn JH, Roux S, Adriaenssens EM, et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat Biotechnol. 2019;37:632–9.
    Google Scholar 
    Hao L, Bize A, Conteau D, Chapleur O, Courtois S, Kroff P, et al. New insights into the key microbial phylotypes of anaerobic sludge digesters under different operational conditions. Water Res. 2016;102:158–69.CAS 
    PubMed 

    Google Scholar 
    Bedoya K, Hoyos O, Zurek E, Cabarcas F, Alzate JF. Annual microbial community dynamics in a full-scale anaerobic sludge digester from a wastewater treatment plant in Colombia. Sci Total Environ. 2020;726:138479.CAS 
    PubMed 

    Google Scholar 
    Murphy KC, Fenton AC, Poteete AR. Sequence of the bacteriophage P22 Anti-RecBCD (abc) genes and properties of P22 abc region deletion mutants. Virology. 1987;160:456–64.CAS 
    PubMed 

    Google Scholar 
    Millman A, Bernheim A, Stokar-Avihail A, Fedorenko T, Voichek M, Leavitt A, et al. Bacterial retrons function in anti-phage defense. Cell. 2020;183:1551–61.CAS 
    PubMed 

    Google Scholar 
    Pawluk A, Davidson AR, Maxwell KL. Anti-CRISPR: discovery, mechanism and function. Nat Rev Microbiol. 2018;16:12–7.CAS 
    PubMed 

    Google Scholar 
    Jonge PA, de, Nobrega FL, Brouns SJJ, Dutilh BE. Molecular and evolutionary determinants of bacteriophage host range. Trends Microbiol. 2018;27:51–63.PubMed 

    Google Scholar 
    Daly RA, Roux S, Borton MA, Morgan DM, Johnston MD, Booker AE, et al. Viruses control dominant bacteria colonizing the terrestrial deep biosphere after hydraulic fracturing. Nat Microbiol. 2019;4:352–61.CAS 
    PubMed 

    Google Scholar 
    Salmond GPC, Fineran PC. A century of the phage: past, present and future. Nat Rev Microbiol. 2015;13:777–86.CAS 
    PubMed 

    Google Scholar 
    Rastogi S, Liberles DA. Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evol Biol. 2005;5:28.PubMed 
    PubMed Central 

    Google Scholar 
    Petitjean C, Makarova KS, Wolf YI, Koonin EV. Extreme deviations from expected evolutionary rates in archaeal protein families. Genome Biol Evol. 2017;9:2791–811.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Anderson CL, Sullivan MB, Fernando SC. Dietary energy drives the dynamic response of bovine rumen viral communities. Microbiome. 2017;5:155.PubMed 
    PubMed Central 

    Google Scholar 
    Gao S-M, Schippers A, Chen N, Yuan Y, Zhang M-M, Li Q, et al. Depth-related variability in viral communities in highly stratified sulfidic mine tailings. Microbiome. 2020;8:89.PubMed 
    PubMed Central 

    Google Scholar 
    Mara P, Vik D, Pachiadaki MG, Suter EA, Poulos B, Taylor GT, et al. Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline. ISME J. 2020;14:3079–92.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pfennig N, Widdel F, Trüper HG. The prokaryotes, A handbook on habitats, isolation, and identification of bacteria. Springer-Verlag, Berlin, Germany. 1981.Moran MA, Durham BP. Sulfur metabolites in the pelagic ocean. Nat Rev Microbiol. 2019;17:665–78.CAS 
    PubMed 

    Google Scholar 
    Kumar S, Cheng X, Klimasauskas S, Sha M, Posfai J, Roberts RJ, et al. The DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 1994;22:1–10.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ashcroft AE, Lago H, Macedo JMB, Horn WT, Stonehouse NJ, Stockley PG. Engineering thermal stability in RNA phage capsids via disulphide bonds. J Nanosci Nanotechno. 2005;5:2034–41.CAS 

    Google Scholar 
    Walter M, Fiedler C, Grassl R, Biebl M, Rachel R, Hermo-Parrado XL, et al. Structure of the receptor-binding protein of bacteriophage Det7: a podoviral tail spike in a Myovirus. J Virol. 2008;82:2265–73.CAS 
    PubMed 

    Google Scholar 
    Shai Y. Mode of action of membrane active antimicrobial peptides. Peptide Sci. 2002;66:236–48.CAS 

    Google Scholar 
    Thevissen K, Ferket KKA, François IEJA, Cammue BPA. Interactions of antifungal plant defensins with fungal membrane components. Peptides. 2003;24:1705–12.CAS 
    PubMed 

    Google Scholar 
    Broderick JB, Duffus BR, Duschene KS, Shepard EM. Radical S-adenosylmethionine enzymes. Chem Rev. 2014;114:4229–317.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wildschutte H, Preheim SP, Hernandez Y, Polz MF. O‐antigen diversity and lateral transfer of the wbe region among Vibrio splendidus isolates. Environ Microbiol. 2010;12:2977–87.CAS 
    PubMed 

    Google Scholar 
    Samuel G, Reeves P. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohyd Res. 2003;338:2503–19.CAS 

    Google Scholar 
    Polz MF, Alm EJ, Hanage WP. Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 2013;29:170–5.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Markine-Goriaynoff N, Gillet L, Etten JLV, Korres H, Verma N, Vanderplasschen A. Glycosyltransferases encoded by viruses. J Gen Virol. 2004;85:2741–54.CAS 
    PubMed 

    Google Scholar 
    Clifford JC, Rapicavoli JN, Roper MC. A rhamnose-rich O-antigen mediates adhesion, virulence, and host colonization for the xylem-limited phytopathogen Xylella fastidiosa. Mol Plant-microbe Interac. 2013;26:676–85.CAS 

    Google Scholar 
    Trueba G, Zapata S, Madrid K, Cullen P, Haake D. Cell aggregation: a mechanism of pathogenic Leptospira to survive in fresh water. Int Microbiol Official J Span Soc Microbiol. 2004;7:35–40.
    Google Scholar 
    Trunk T, Khalil HS, Leo JC. Norway BCSG Section for Genetics and Evolutionary Biology, Department of Biosciences, University of Oslo, Oslb,. Bacterial autoaggregation. Aims Microbiol. 2018;4:140–164.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Guan S, Bastin DA, Verma NK. Functional analysis of the O antigen glucosylation gene cluster of Shigella flexneri bacteriophage SfX. Microbiology. 1999;145:1263–73.CAS 
    PubMed 

    Google Scholar 
    Rakhuba DV, Kolomiets EI, Dey ES, Novik GI. Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol. 2010;59:145–55.CAS 
    PubMed 

    Google Scholar 
    Silva JB, Storms Z, Sauvageau D. Host receptors for bacteriophage adsorption. FEMS Microbiol Lett. 2016;363:fnw002.
    Google Scholar 
    Tsuzuki K, Kimura K, Fujii N, Yokosawa N, Oguma K. The complete nucleotide sequence of the gene coding for the nontoxic-nonhemagglutinin component of Clostridium botulinum type C progenitor toxin. Biochem Bioph Res Co. 1992;183:1273–9.CAS 

    Google Scholar 
    Enav H, Mandel-Gutfreund Y, Béjà O. Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis. Microbiome. 2014;2:9.PubMed 
    PubMed Central 

    Google Scholar 
    Emerson JB, Roux S, Brum JR, Bolduc B, Woodcroft BJ, Jang HB, et al. Host-linked soil viral ecology along a permafrost thaw gradient. Nat Microbiol. 2018;3:870–80.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jin M, Guo X, Zhang R, Qu W, Gao B, Zeng R. Diversities and potential biogeochemical impacts of mangrove soil viruses. Microbiome. 2019;7:58.PubMed 
    PubMed Central 

    Google Scholar 
    Anderson RE, Reveillaud J, Reddington E, Delmont TO, Eren AM, McDermott JM, et al. Genomic variation in microbial populations inhabiting the marine subseafloor at deep-sea hydrothermal vents. Nat Commun. 2017;8:1114.PubMed 
    PubMed Central 

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

    Google Scholar 
    Kopylova E, Noé L, Touzet H. SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28:3211–7.CAS 
    PubMed 

    Google Scholar 
    Lu J, Salzberg SL. Ultrafast and accurate 16S rRNA microbial community analysis using Kraken 2. Microbiome. 2020;8:124.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lu J, Breitwieser FP, Thielen P, Salzberg SL. Bracken: estimating species abundance in metagenomics data. Peerj Comput Sci. 2017;3:e104.
    Google Scholar 
    Beghini F, McIver LJ, Blanco-Míguez A, Dubois L, Asnicar F, Maharjan S, et al. Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3. Elife. 2021;10:e65088.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat methods. 2012;9:357–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9.PubMed 
    PubMed Central 

    Google Scholar 
    Wu Y-W, 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 

    Google Scholar 
    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.PubMed 
    PubMed Central 

    Google Scholar 
    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;3:1043–55.
    Google Scholar 
    Olm MR, Brown CT, Brooks B, Banfield JF. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864–8.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics. 2019;6:1925–7.
    Google Scholar 
    Guo J, Bolduc B, Zayed AA, Varsani A, Dominguez-Huerta G, Delmont TO, et al. VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome. 2021;9:37.PubMed 
    PubMed Central 

    Google Scholar 
    Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature. 2016;537:689–93.CAS 
    PubMed 

    Google Scholar 
    Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, et al. Uncovering Earth’s virome. Nature. 2016;536:425–30.CAS 
    PubMed 

    Google Scholar 
    Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J, Néron B, et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 2018;46:W246–W251.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lowe TM, Eddy SR. tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence. Nucleic Acids Res. 1997;25:955–64.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.
    Google Scholar 
    Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M, Goto S, et al. KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics. 2019;36:2251–52.PubMed Central 

    Google Scholar 
    Mistry J, Bateman A, Finn RD. Predicting active site residue annotations in the Pfam database. BMC Bioinform. 2007;8:298.
    Google Scholar 
    Shaffer M, Borton MA, McGivern BB, Zayed AA, La Rosa SL, Solden LM, et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 2020;48:8883–900.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pratama AA, Bolduc B, Zayed AA, Zhong Z-P, Guo J, Vik DR, et al. Expanding standards in viromics: in silico evaluation of dsDNA viral genome identification, classification, and auxiliary metabolic gene curation. Peerj. 2021;9:e11447.PubMed 
    PubMed Central 

    Google Scholar 
    Zimmermann L, Stephens A, Nam S-Z, Rau D, Kübler J, Lozajic M, et al. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol. 2018;430:2237–43.CAS 
    PubMed 

    Google Scholar 
    Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015;10:845–58.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinform Oxf Engl. 2011;27:1009–10.CAS 

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

    Google Scholar 
    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 

    Google Scholar 
    Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Haeseler Avon, et al. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:gkab301-.
    Google Scholar 
    Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP, et al. Community-wide analysis of microbial genome sequence signatures. Genome Biol. 2009;10:R85–R85.PubMed 
    PubMed Central 

    Google Scholar  More

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    Microbiomes of bloom-forming Phaeocystis algae are stable and consistently recruited, with both symbiotic and opportunistic modes

    Moran MA, Kujawinski EB, Stubbins A, Fatland R, Aluwihare LI, Buchan A, et al. Deciphering ocean carbon in a changing world. Proc Natl Acad Sci USA 2016;113:3143–51.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Seymour JR, Amin SA, Raina J-B, Stocker R Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol. 2017;2:17065.Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science. 2011;332:1097–1100.CAS 
    PubMed 

    Google Scholar 
    Cirri E, Pohnert G. Algae-bacteria interactions that balance the planktonic microbiome. N. Phytol. 2019;223:100–6.
    Google Scholar 
    Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature. 2015;522:98–101.CAS 
    PubMed 

    Google Scholar 
    Grant MAA, Kazamia E, Cicuta P, Smith AG. Direct exchange of vitamin B12 is demonstrated by modelling the growth dynamics of algal-bacterial cocultures. ISME J. 2014;8:1418–27.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bertrand EM, McCrow JP, Moustafa A, Zheng H, McQuaid JB, Delmont TO, et al. Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proc Natl Acad Sci USA 2015;112:9938–43.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Durham BP, Sharma S, Luo H, Smith CB, Amin SA, Bender SJ, et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci USA 2015;112:453–7.CAS 
    PubMed 

    Google Scholar 
    Suleiman M, Zecher K, Yücel O, Jagmann N, Philipp B. Interkingdom cross-feeding of ammonium from marine methylamine-degrading bacteria to the diatom Phaeodactylum tricornutum. Appl Environ Microbiol. 2016;82:7113–22.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem. 2011;3:331–5.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ratnarajah L, Blain S, Boyd PW, Fourquez M, Obernosterer I, Tagliabue A. Resource colimitation drives competition between phytoplankton and bacteria in the Southern Ocean. Geophys Res Lett. 2021;48:e2020GL088369.PubMed 
    PubMed Central 

    Google Scholar 
    Løvdal T, Eichner C, Grossart H-P, Carbonnel V, Chou L, Martin-Jézéquel V, et al. Competition for inorganic and organic forms of nitrogen and phosphorous between phytoplankton and bacteria during an Emiliania huxleyi spring bloom. Biogeosciences. 2008;5:371–83.
    Google Scholar 
    Arrigo KR, Robinson DH, Worthen DL, Dunbar RB, DiTullio GR, VanWoert M, et al. Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science. 1999;283:365–7.CAS 
    PubMed 

    Google Scholar 
    Geider R, La Roche J. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol. 2002;37:1–17.
    Google Scholar 
    Smayda TJ. Normal and accelerated sinking of phytoplankton in the sea. Mar Geol. 1971;11:105–22.
    Google Scholar 
    Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tréguer P, Bowler C, Moriceau B, Dutkiewicz S, Gehlen M, Aumont O, et al. Influence of diatom diversity on the ocean biological carbon pump. Nat Geosci. 2018;11:27–37.
    Google Scholar 
    Ferrer-González FX, Widner B, Holderman NR, Glushka J, Edison AS, Kujawinski EB, et al. Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy. ISME J. 2021;15:762–73.PubMed 

    Google Scholar 
    Mönnich J, Tebben J, Bergemann J, Case R, Wohlrab S, Harder T. Niche-based assembly of bacterial consortia on the diatom Thalassiosira rotula is stable and reproducible. ISME J. 2020;14:1614–25.PubMed 
    PubMed Central 

    Google Scholar 
    Shibl AA, Isaac A, Ochsenkühn MA, Cárdenas A, Fei C, Behringer G, et al. Diatom modulation of select bacteria through use of two unique secondary metabolites. Proc Natl Acad Sci USA 2020;117:27445–55.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res. 2005;53:43–66.CAS 

    Google Scholar 
    Peperzak L, Colijn F, Gieskes WWC, Peeters JCH. Development of the diatom-Phaeocystis spring bloom in the Dutch coastal zone of the North Sea: the silicon depletion versus the daily irradiance threshold hypothesis. J Plankton Res. 1998;20:517–37.
    Google Scholar 
    Hai D-N, Lam N-N, Dippner JW. Development of Phaeocystis globosa blooms in the upwelling waters of the south central coast of Viet Nam. J Mar Syst. 2010;83:253–61.
    Google Scholar 
    Wang X, Song H, Wang Y, Chen N. Research on the biology and ecology of the harmful algal bloom species Phaeocystis globosa in China: Progresses in the last 20 years. Harmful Algae. 2021;107:102057.PubMed 

    Google Scholar 
    Jiang M, Borkman DG, Scott Libby P, Townsend DW, Zhou M. Nutrient input and the competition between Phaeocystis pouchetii and diatoms in Massachusetts Bay spring bloom. J Mar Syst. 2014;134:29–44.
    Google Scholar 
    Nissen C, Vogt M. Factors controlling the competition between Phaeocystis and diatoms in the Southern Ocean and implications for carbon export fluxes. Biogeosciences. 2021;18:251–83.CAS 

    Google Scholar 
    Mars Brisbin M, Mitarai S. Differential gene expression supports a resource-intensive, defensive role for colony production in the bloom-forming haptophyte, Phaeocystis globosa. J Eukaryot Microbiol. 2019;66:788–801.PubMed 
    PubMed Central 

    Google Scholar 
    Zhu Z, Meng R, Smith WO Jr, Doan-Nhu H, Nguyen-Ngoc L, Jiang X. Bacterial composition associated with giant colonies of the harmful algal species Phaeocystis globosa. Front Microbiol. 2021;12:737484.PubMed 
    PubMed Central 

    Google Scholar 
    Delmont TO, Hammar KM, Ducklow HW, Yager PL, Post AF. Phaeocystis antarctica blooms strongly influence bacterial community structures in the Amundsen Sea polynya. Front Microbiol. 2014;5:646.PubMed 
    PubMed Central 

    Google Scholar 
    Verity PG, Whipple SJ, Nejstgaard JC, Alderkamp A-C. Colony size, cell number, carbon and nitrogen contents of Phaeocystis pouchetii from western Norway. J Plankton Res. 2007;29:359–67.
    Google Scholar 
    Alderkamp A-C, Buma AGJ, van Rijssel M. The carbohydrates of Phaeocystis and their degradation in the microbial food web. Biogeochemistry. 2007;83:99–118.CAS 

    Google Scholar 
    Smriga S, Fernandez VI, Mitchell JG, Stocker R. Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria. Proc Natl Acad Sci USA 2016;113:1576–81.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Mühlenbruch M, Grossart H-P, Eigemann F, Voss M. Mini-review: Phytoplankton-derived polysaccharides in the marine environment and their interactions with heterotrophic bacteria. Environ Microbiol. 2018;20:2671–85.PubMed 

    Google Scholar 
    Raina J-B, Fernandez V, Lambert B, Stocker R, Seymour JR. The role of microbial motility and chemotaxis in symbiosis. Nat Rev Microbiol. 2019;17:284–94.CAS 
    PubMed 

    Google Scholar 
    Solomon CM, Lessard EJ, Keil RG, Foy MS. Characterization of extracellular polymers of Phaeocystis globosa and P. antarctica. Mar Ecol Prog Ser. 2003;250:81–89.CAS 

    Google Scholar 
    Shen P, Qi Y, Wang Y, Huang L. Phaeocystis globosa Scherffel, a harmful microalga, and its production of dimethylsulfoniopropionate. Chin J Oceano Limnol. 2011;29:869–73.CAS 

    Google Scholar 
    Louca S, Polz MF, Mazel F, Albright MBN, Huber JA, O’Connor MI, et al. Function and functional redundancy in microbial systems. Nat Ecol Evol. 2018;2:936–43.PubMed 

    Google Scholar 
    Wang J, Bouwman AF, Liu X, Beusen AHW, Van Dingenen R, Dentener F, et al. Harmful algal blooms in chinese coastal waters will persist due to perturbed nutrient ratios. Environ Sci Technol Lett. 2021;8:276–84.CAS 

    Google Scholar 
    Foster RA, Kuypers MMM, Vagner T, Paerl RW, Musat N, Zehr JP. Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J. 2011;5:1484–93.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Helliwell KE. The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. N. Phytol. 2017;216:62–68.CAS 

    Google Scholar 
    Bertrand EM, Saito MA, Rose JM, Riesselman CR, Lohan MC, Noble AE, et al. Vitamin B12 and iron colimitation of phytoplankton growth in the Ross Sea. Limnol Oceanogr. 2007;52:1079–93.CAS 

    Google Scholar 
    Tang YZ, Koch F, Gobler CJ. Most harmful algal bloom species are vitamin B1 and B12 auxotrophs. Proc Natl Acad Sci USA 2010;107:20756–61.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature. 2005;438:90–93.CAS 
    PubMed 

    Google Scholar 
    Guillard RRL, Hargraves PE. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia. 1993;32:234–6.
    Google Scholar 
    Hamilton PB, Lefebvre KE, Bull RD. Single cell PCR amplification of diatoms using fresh and preserved samples. Front Microbiol. 2015;6:1084.PubMed 
    PubMed Central 

    Google Scholar 
    dos Reis MC, Romac S, Le Gall F, Marie D, Frada MJ, Koplovitz G, et al. Exploring the phycosphere of Emiliania huxleyi: from bloom dynamics to microbiome assembly experiments. bioRxiv 2022;02;21:481256.Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Glo FO, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6.
    Google Scholar 
    Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018;6:90.PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team. R: A language and environment for statistical computing. 2018. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.Mcmurdie PJ, Holmes S phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013;8:e61217.Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ. Microbiome datasets are compositional: and this is not optional. Front Microbiol. 2017;8:2224.PubMed 
    PubMed Central 

    Google Scholar 
    Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R package version. 2019;2:5–4.
    Google Scholar 
    Ares Á, Brisbin MM, Sato KN, Martín JP, Iinuma Y, Mitarai S. Extreme storms cause rapid but short-lived shifts in nearshore subtropical bacterial communities. Environ Microbiol. 2020;22:4571–88.CAS 
    PubMed 

    Google Scholar 
    Radwan SSA, Al-Mailem DM, Kansour MK. Gelatinizing oil in water and its removal via bacteria inhabiting the gels. Sci Rep. 2017;7:13975.PubMed 
    PubMed Central 

    Google Scholar 
    Behringer G, Ochsenkühn MA, Fei C, Fanning J, Koester JA, Amin SA. Bacterial communities of diatoms display strong conservation across strains and time. Front Microbiol. 2018;9:659.PubMed 
    PubMed Central 

    Google Scholar 
    Glaeser SP, Imani J, Alabid I, Guo H, Kumar N, Kämpfer P, et al. Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica. ISME J. 2016;10:871–84.PubMed 

    Google Scholar 
    Chakraborty U, Chakraborty BN, Dey PL, Chakraborty AP, Sarkar J. Biochemical responses of wheat plants primed with Ochrobactrum pseudogrignonense and subjected to salinity stress. Agric Res. 2019;8:427–40.CAS 

    Google Scholar 
    Johnson WM, Alexander H, Bier RL, Miller DR, Muscarella ME, Pitz KJ, et al. Auxotrophic interactions: a stabilizing attribute of aquatic microbial communities? FEMS Microbiol Ecol. 2020;96;11:fiaa115.Ajani PA, Kahlke T, Siboni N, Carney R, Murray SA, Seymour JR. The Microbiome of the cosmopolitan diatom Leptocylindrus reveals significant spatial and temporal variability. Front Microbiol. 2018;9:2758.PubMed 
    PubMed Central 

    Google Scholar 
    Connor EF, McCoy ED. The statistics and biology of the species-area relationship. Am Nat. 1979;113:791–833.
    Google Scholar 
    Hamm CE, Simson DA, Merkel R, Smetacek V. Colonies of Phaeocystis globosa are protected by a thin but tough skin. Mar Ecol Prog Ser. 1999;187:101–11.
    Google Scholar 
    Geddes BA, Paramasivan P, Joffrin A, Thompson AL, Christensen K, Jorrin B, et al. Engineering transkingdom signalling in plants to control gene expression in rhizosphere bacteria. Nat Commun. 2019;10:3430.PubMed 
    PubMed Central 

    Google Scholar 
    Sieburth JM. Acrylic acid, an‘ antibiotic’ principle in Phaeocystis blooms in Antarctic waters. Science. 1960;132:676–7.CAS 
    PubMed 

    Google Scholar 
    Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinform. 2009;10:421.
    Google Scholar 
    Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2016;44:D67–72.CAS 
    PubMed 

    Google Scholar 
    López-Pérez M, Gonzaga A, Martin-Cuadrado A-B, Onyshchenko O, Ghavidel A, Ghai R, et al. Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph. Sci Rep. 2012;2:696.PubMed 
    PubMed Central 

    Google Scholar 
    Diner RE, Schwenck SM, McCrow JP, Zheng H, Allen AE. Genetic manipulation of competition for nitrate between heterotrophic bacteria and diatoms. Front Microbiol. 2016;7:880.PubMed 
    PubMed Central 

    Google Scholar 
    Monteiro RA, Balsanelli E, Wassem R, Marin AM, Brusamarello-Santos LCC, Schmidt MA, et al. Herbaspirillum-plant interactions: microscopical, histological and molecular aspects. Plant Soil. 2012;356:175–96.CAS 

    Google Scholar 
    Bastián F, Cohen A, Piccoli P, Luna V, Baraldi R. Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regul. 1998;24:7–11.
    Google Scholar 
    Gyaneshwar P, James EK, Reddy PM. Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium‐tolerant rice varieties. N. Phytol. 2002;154:131–45.CAS 

    Google Scholar 
    Guo H, Yang Y, Liu K, Xu W, Gao J, Duan H, et al. Comparative genomic analysis of Delftia tsuruhatensis MTQ3 and the identification of functional NRPS genes for siderophore production. Biomed Res Int. 2016;2016:3687619.PubMed 
    PubMed Central 

    Google Scholar 
    Vásquez-Piñeros MA, Martínez-Lavanchy PM, Jehmlich N, Pieper DH, Rincón CA, Harms H, et al. Delftia sp. LCW, a strain isolated from a constructed wetland shows novel properties for dimethylphenol isomers degradation. BMC Microbiol. 2018;18:108.PubMed 
    PubMed Central 

    Google Scholar 
    Riegman R, Noordeloos AAM, Cadée GC. Phaeocystis blooms and eutrophication of the continental coastal zones of the North Sea. Mar Biol. 1992;112:479–84.
    Google Scholar 
    Sañudo-Wilhelmy SA, Cutter LS, Durazo R, Smail EA, Gómez-Consarnau L, Webb EA, et al. Multiple B-vitamin depletion in large areas of the coastal ocean. Proc Natl Acad Sci USA 2012;109:14041–5.PubMed 
    PubMed Central 

    Google Scholar 
    Gobler CJ, Norman C, Panzeca C, Taylor GT, Sañudo-Wilhelmy SA. Effect of B-vitamins (B1, B12) and inorganic nutrients on algal bloom dynamics in a coastal ecosystem. Aquat Micro Ecol. 2007;49:181–94.
    Google Scholar 
    Gómez-Consarnau L, Sachdeva R, Gifford SM, Cutter LS, Fuhrman JA, Sañudo-Wilhelmy SA, et al. Mosaic patterns of B-vitamin synthesis and utilization in a natural marine microbial community. Environ Microbiol. 2018;20:2809–23.PubMed 

    Google Scholar 
    Bertrand EM, Saito MA, Jeon YJ, Neilan BA. Vitamin B12 biosynthesis gene diversity in the Ross Sea: the identification of a new group of putative polar B12 biosynthesizers. Environ Microbiol. 2011;13:1285–98.CAS 
    PubMed 

    Google Scholar  More

  • in

    Morphological variation and reproductive isolation in the Hetaerina americana species complex

    Coyne, J. A. & Orr, H. A. Speciation (Sinauer Associates, 2004).
    Google Scholar 
    Gröning, J. & Hochkirch, A. Reproductive interference between animal species. Q. Rev. Biol. 83, 257–282 (2008).PubMed 

    Google Scholar 
    Grether, G. F., Peiman, K. S., Tobias, J. A. & Robinson, B. W. Causes and consequences of behavioral interference between species. Trends Ecol. Evol. 32, 760–772 (2017).PubMed 

    Google Scholar 
    Hettyey, A. & Pearman, P. B. Social environment and reproductive interference affect reproductive success in the frog Rana latastei. Behav. Ecol. 14, 294–300 (2003).
    Google Scholar 
    Kyogoku, D. & Sota, T. A generalized population dynamics model for reproductive interference with absolute density dependence. Sci. Rep. 7, 257–258 (2017).
    Google Scholar 
    Anderson, C. N. & Grether, G. F. Multiple routes to reduced interspecific territorial fighting in Hetaerina damselflies. Behav. Ecol. 22, 527–534 (2011).
    Google Scholar 
    Hochkirch, A., Gröning, J. & Bücker, A. Sympatry with the devil: Reproductive interference could hamper species coexistence. J. Anim. Ecol. 76, 633–642 (2007).PubMed 

    Google Scholar 
    Pfennig, K. S. & Pfennig, D. W. Character displacement: Ecological and reproductive responses to a common evolutionary problem. Q. Rev. Biol. 84, 253–276 (2009).PubMed 
    PubMed Central 

    Google Scholar 
    Garrison, R. A synopsis of the genus Hetaerina with description of four new species (Odonata: Calopterygidae). Trans. Am. Entomol. Soc. 116, 175–259 (1990).
    Google Scholar 
    Grether, G. F., Drury, J. P., Berlin, E. & Anderson, C. N. The role of wing coloration in sex recognition and competitor recognition in rubyspot damselflies (Hetaerina spp.). Ethology 121, 674–685 (2015).
    Google Scholar 
    Drury, J. P. et al. A general explanation for the persistence of reproductive interference. Am. Nat. 194, 268–275 (2019).PubMed 

    Google Scholar 
    Cabezas Castillo, M. B. & Grether, G. F. Why are female color polymorphisms rare in territorial damselflies?. Ethology 124, 667–673 (2018).
    Google Scholar 
    Drury, J. P. & Grether, G. F. Interspecific aggression, not interspecific mating, drives character displacement in the wing coloration of male rubyspot damselflies (Hetaerina). Proc. R. Soc. B Biol. Sci. 281, 20141737 (2014).CAS 

    Google Scholar 
    Grether, G. F. Intersexual competition alone favors a sexually dimorphic ornament in the rubyspot damselfly Hetaerina americana. Evolution (N. Y.) 50, 1949 (1996).
    Google Scholar 
    McEachin, S., Drury, J. P., Anderson, C. N. & Grether, G. F. Mechanisms of reduced interspecific interference between territorial species. Behav. Ecol. 33, 126–136 (2022).
    Google Scholar 
    Vega-Sánchez, Y. M., Mendoza-Cuenca, L. F. & González-Rodríguez, A. Complex evolutionary history of the American Rubyspot damselfly, Hetaerina americana (Odonata): Evidence of cryptic speciation. Mol. Phylogenet. Evol. 139, 106536 (2019).PubMed 

    Google Scholar 
    Vega-Sánchez, Y. M., Mendoza-Cuenca, L. F. & González-Rodríguez, A. Hetaerina calverti (Odonata: Zygoptera: Calopterygidae) sp. Nov., a new cryptic species of the American Rubyspot complex. Zootaxa 4766, 485–497 (2020).
    Google Scholar 
    Paulson, D. R. Reproductive isolation in damselflies. Syst. Zool. 23, 40–49 (1974).
    Google Scholar 
    Sánchez-Guillén, R. A., Córdoba-Aguilar, A., Cordero-Rivera, A. & Wellenreuther, M. Rapid evolution of prezygotic barriers in non-territorial damselflies. Biol. J. Linn. Soc. 113, 485–496 (2014).
    Google Scholar 
    Svensson, E. I. & Waller, J. T. Ecology and sexual selection: Evolution of wing pigmentation in calopterygid damselflies in relation to latitude, sexual dimorphism, and speciation. Am. Nat. 182, E174–E195 (2013).PubMed 

    Google Scholar 
    Sánchez-Herrera, M., Beatty, C. D., Nunes, R., Salazar, C. & Ware, J. L. An exploration of the complex biogeographical history of the neotropical banner-wing damselflies (Odonata: Polythoridae). BMC Evol. Biol. 20, 74 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Battin, T. J. The odonate mating system, communication, and sexual selection: A review. Boll. Zool. 60, 353–360 (1993).
    Google Scholar 
    Drury, J. P., Okamoto, K. W., Anderson, C. N. & Grether, G. F. Reproductive interference explains persistence of aggression between species. Proc. R. Soc. B Biol. Sci. 282, 20142256 (2015).
    Google Scholar 
    Svensson, E. I., Karlsson, K., Friberg, M. & Eroukhmanoff, F. Gender differences in species recognition and the evolution of asymmetric sexual isolation. Curr. Biol. 17, 1943–1947 (2007).CAS 
    PubMed 

    Google Scholar 
    McPeek, M. A., Symes, L. B., Zong, D. M. & McPeek, C. L. Species recognition and patterns of population variation in the reproductive structures of a damselfly genus. Evolution (N. Y.) 65, 419–428 (2011).
    Google Scholar 
    Nagel, L. & Schluter, D. Body size, natural selection, and speciation in sticklebacks. Evolution (N. Y.) 52, 209–218 (1998).
    Google Scholar 
    Baube, C. L. Body size and the maintenance of reproductive isolation in stickleback, genus Gasterosteus. Ethology 114, 1122–1134 (2008).
    Google Scholar 
    Head, M. L., Kozak, G. M. & Boughman, J. W. Female mate preferences for male body size and shape promote sexual isolation in threespine sticklebacks. Ecol. Evol. 3, 2183–2196 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Serrano-Meneses, M. A., López-García, K. & Carrillo-Muñoz, A. I. Assortative mating by size in the American rubyspot damselfly (Hetaerina americana). J. Insect Behav. 31, 585–598 (2018).
    Google Scholar 
    Kopp, M. et al. Mechanisms of assortative mating in speciation with gene flow: Connecting theory and empirical research. Am. Nat. 191, 1–20 (2018).PubMed 

    Google Scholar 
    Class, B. & Dingemanse, N. J. A variance partitioning perspective of assortative mating: Proximate mechanisms and evolutionary implications. J. Evol. Biol. 35, 483–490 (2022).PubMed 

    Google Scholar 
    Corbet, P. S. A Biology of Dragonflies 247 (Witherby, 1962).
    Google Scholar 
    Grether, G. F. Sexual selection and survival selection on wing coloration and body size in the Rubyspot damselfly Hetaerina americana. Evolution (N. Y.) 50, 1939 (1996).
    Google Scholar 
    Raihani, G., Serrano-Meneses, M. A. & Córdoba-Aguilar, A. Male mating tactics in the American rubyspot damselfly: Territoriality, nonterritoriality and switching behaviour. Anim. Behav. 75, 1851–1860 (2008).
    Google Scholar 
    Serrano-Meneses, M. A., Córdoba-Aguilar, A., Méndez, V., Layen, S. J. & Székely, T. Sexual size dimorphism in the American rubyspot: Male body size predicts male competition and mating success. Anim. Behav. 73, 987–997 (2007).
    Google Scholar 
    Contreras-Garduño, J., Buzatto, B. A., Abundis, L., Nájera-Cordero, K. & Córdoba-Aguilar, A. Wing colour properties do not reflect male condition in the American rubyspot (Hetaerina americana). Ethology 113, 944–952 (2007).
    Google Scholar 
    Serrano-Meneses, M. A., Córdoba-Aguilar, A., Azpilicueta-Amorín, M., González-Soriano, E. & Székely, T. Sexual selection, sexual size dimorphism and Rensch’s rule in Odonata. J. Evol. Biol. 21, 1259–1273 (2008).CAS 
    PubMed 

    Google Scholar 
    Betts, C. R. & Wootton, R. J. Wing shape and flight behaviour in butterflies (Lepidoptera: Papilionoidea and Hesperioidea): A preliminary analysis. J. Exp. Biol. 138, 271–288 (1988).
    Google Scholar 
    Outomuro, D. & Johansson, F. The effects of latitude, body size, and sexual selection on wing shape in a damselfly. Biol. J. Linn. Soc. 102, 263–274 (2011).
    Google Scholar 
    Outomuro, D., Adams, D. C. & Johansson, F. The evolution of wing shape in ornamented-winged damselflies (Calopterygidae, Odonata). Evol. Biol. 40, 300–309 (2013).
    Google Scholar 
    Córdoba-Aguilar, Raihani, Serrano-Meneses, & Contreras-Garduño,. The lek mating system of Hetaerina damselflies (Insecta: Calopterygidae). Behaviour 146, 189–207 (2009).
    Google Scholar 
    Córdoba-Aguilar, A. Adult survival and movement in males of the damselfly Hetaerina cruentata (Odonata: Calopterygidae). Florida Entomol. 77, 256 (1994).
    Google Scholar 
    Peakall, R. & Smouse, P. E. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—An update. Bioinformatics 28, 2537–2539 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chapuis, M.-P. & Estoup, A. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621–631 (2007).CAS 
    PubMed 

    Google Scholar 
    Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).PubMed 

    Google Scholar 
    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620 (2005).CAS 
    PubMed 

    Google Scholar 
    Troscianko, J. & Stevens, M. Image calibration and analysis toolbox—A free software suite for objectively measuring reflectance, colour and pattern. Methods Ecol. Evol. 6, 1320–1331 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. https://doi.org/10.18637/jss.v067.i01 (2015).Article 

    Google Scholar 
    Adams, D. C. & Otárola-Castillo, E. Geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).
    Google Scholar 
    Viscosi, V. & Cardini, A. Correction: Leaf morphology, taxonomy and geometric morphometrics: A simplified protocol for beginners. PLoS ONE https://doi.org/10.1371/annotation/bc347abe-8d03-4553-8754-83f41a9d51ae (2012).Article 
    PubMed Central 

    Google Scholar 
    Maia, R., Gruson, H., Endler, J. A. & White, T. E. PAVO 2: New tools for the spectral and spatial analysis of colour in R. Methods Ecol. Evol. 10, 1097–1107 (2019).
    Google Scholar 
    Vorobyev, M. & Osorio, D. Receptor noise as a determinant of colour thresholds. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265, 351–358 (1998).CAS 

    Google Scholar 
    Outomuro, D., Söderquist, L., Johansson, F., Ödeen, A. & Nordström, K. The price of looking sexy: Visual ecology of a three-level predator–prey system. Funct. Ecol. 31, 707–718 (2017).
    Google Scholar 
    Laughlin, S. B. The sensitivities of dragonfly photoreceptors and the voltage gain of transduction. J. Comp. Physiol. A 111, 221–247 (1976).
    Google Scholar 
    Endler, J. A. The color of light in forests and its implications. Ecol. Monogr. 63, 1–27 (1993).
    Google Scholar 
    Vorobyev, M., Brandt, R., Peitsch, D., Laughlin, S. B. & Menzel, R. Colour thresholds and receptor noise: Behaviour and physiology compared. Vision Res. 41, 639–653 (2001).CAS 
    PubMed 

    Google Scholar 
    Renoult, J. P., Kelber, A. & Schaefer, H. M. Colour spaces in ecology and evolutionary biology. Biol. Rev. 92, 292–315 (2017).PubMed 

    Google Scholar 
    Zelditch, M. L., Swiderski, D. L., Sheets, H. D. & Fink, W. L. Geometric Morphometrics for Biologists: A Primer Vol. 95, 443 (Elsevier Academic Press, 2004).MATH 

    Google Scholar 
    Rohlf, F. J. TpsDig, Digitize Landmarks and Outlines v. 2.0 (Department of Ecology and Evolution, State University of New York at Stony Brook, 2004).
    Google Scholar  More

  • in

    Unique metabolism of different glucosinolates in larvae and adults of a leaf beetle specialised on Brassicaceae

    War, A. R. et al. Mechanisms of plant defense against insect herbivores. Plant Signal. Behav. 7, 1306–1320 (2012).Article 

    Google Scholar 
    Pentzold, S., Zagrobelny, M., Roelsgaard, P. S., Møller, B. L. & Bak, S. The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence. PLoS ONE 9, e91337. https://doi.org/10.1371/journal.pone.0091337 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Abdalsamee, M. K., Giampa, M., Niehaus, K. & Müller, C. Rapid incorporation of glucosinolates as a strategy used by a herbivore to prevent activation by myrosinases. Insect Biochem. Mol. Biol. 52, 115–123. https://doi.org/10.1016/j.ibmb.2014.07.002 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Winde, I. & Wittstock, U. Insect herbivore counteradaptations to the plant glucosinolate-myrosinase system. Phytochemistry 72, 1566–1575. https://doi.org/10.1016/j.phytochem.2011.01.016 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sporer, T., Körnig, J. & Beran, F. Ontogenetic differences in the chemical defence of flea beetles influence their predation risk. Funct Ecol. 34, 1370–1379. https://doi.org/10.1111/1365-2435.13548 (2020).Article 

    Google Scholar 
    Hammer, T. J. & Moran, N. A. Links between metamorphosis and symbiosis in holometabolous insects. Philos. Trans. R. Soc. B-Biol. Sci. 374, 20190068. https://doi.org/10.1098/rstb.2019.0068 (2019).CAS 
    Article 

    Google Scholar 
    Wäckers, F. L., Romeis, J. & van Rijn, P. Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annu. Rev. Entomol. 52, 301–323. https://doi.org/10.1146/annurev.ento.52.110405.091352 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Altermatt, F. & Pearse, I. S. Similarity and specialization of the larval versus adult diet of european butterflies and moths. Am. Nat. 178, 372–382. https://doi.org/10.1086/661248 (2011).Article 
    PubMed 

    Google Scholar 
    Hammer, T. J., McMillan, W. O. & Fierer, N. Metamorphosis of a butterfly-associated bacterial community. PLoS ONE 9, e86995. https://doi.org/10.1371/journal.pone.0086995 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shukla, S. P., Sanders, J. G., Byrne, M. J. & Pierce, N. E. Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae. Mol. Ecol. 25, 6092–6106. https://doi.org/10.1111/mec.13901 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Blažević, I. et al. Glucosinolate structural diversity, identification, chemical synthesis and metabolism in plants. Phytochemistry 169, 112100. https://doi.org/10.1016/j.phytochem.2019.112100 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Halkier, B. A. & Gershenzon, J. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303–333. https://doi.org/10.1146/annurev.arplant.57.032905.105228 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    Wittstock, U., Kurzbach, E., Herfurth, A. M. & Stauber, E. J. Glucosinolate breakdown. Adv. Botanical Res. – Glucosinolates 80, 125–169. https://doi.org/10.1016/bs.abr.2016.06.006 (2016).CAS 
    Article 

    Google Scholar 
    Jeschke, V., Gershenzon, J. & Vassão, D. G. in Glucosinolates Vol. 80 Advances in Botanical Research (ed S. Kopriva), 199–245 (2016).Sun, R. et al. Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance. eLife 9, e51029, doi:https://doi.org/10.7554/eLife.51029 (2019).Malka, O. et al. Glucosinolate desulfation by the phloem-feeding insect Bemisia tabaci. J. Chem. Ecol. 42, 230–235. https://doi.org/10.1007/s10886-016-0675-1 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Schramm, K., Vassão, D. G., Reichelt, M., Gershenzon, J. & Wittstock, U. Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem. Mol. Biol. 42, 174–182. https://doi.org/10.1016/j.ibmb.2011.12.002 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Beran, F. et al. Phyllotreta striolata flea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system. Proc. Natl. Acad. Sci. USA 111, 7349–7354. https://doi.org/10.1073/pnas.1321781111 (2014).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Beran, F. et al. One pathway is not enough: The cabbage stem flea beetle Psylliodes chrysocephala uses multiple strategies to overcome the glucosinolate-myrosinase defense in its host plants. Front. Plant Sci. 9, 1754. https://doi.org/10.3389/fpls.2018.01754 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Müller, C. et al. Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J. Chem. Ecol. 27, 2505–2516 (2001).Article 

    Google Scholar 
    Ratzka, A., Vogel, H., Kliebenstein, D. J., Mitchell-Olds, T. & Kroymann, J. Disarming the mustard oil bomb. Proc. Natl. Acad. Sci. USA. 99, 11223–11228 (2002).ADS 
    CAS 
    Article 

    Google Scholar 
    Wittstock, U. et al. Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc. Natl. Acad. Sci. USA. 101, 4859–4864 (2004).ADS 
    CAS 
    Article 

    Google Scholar 
    Falk, K. L. & Gershenzon, J. The desert locust, Schistocerca gregaria, detoxifies the glucosinolates of Schouwia purpurea by desulfation. J. Chem. Ecol. 33, 1542–1555. https://doi.org/10.1007/s10886-007-9331-0 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Vanhaelen, N., Haubruge, E., Lognay, G. & Francis, F. Hoverfly glutathione S-transferases and effect of Brassicaceae secondary metabolites. Pestic. Biochem. Phys. 71, 170–177 (2001).CAS 
    Article 

    Google Scholar 
    Friedrichs, J. et al. Novel glucosinolate metabolism in larvae of the leaf beetle Phaedon cochleariae. Insect Biochem. Mol. Biol. 124, 103431. https://doi.org/10.1016/j.ibmb.2020.103431 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Reifenrath, K., Riederer, M. & Müller, C. Leaf surface wax layers of Brassicaceae lack feeding stimulants for Phaedon cochleariae. Entomol. Exp. Appl. 115, 41–50 (2005).CAS 
    Article 

    Google Scholar 
    Cataldi, T. R. I., Lelario, F., Orlando, D. & Bufo, S. A. Collision-induced dissociation of the A+2 isotope ion facilitates glucosinolates structure elucidation by electrospray Ionization-Tandem Mass Spectrometry with a linear Quadrupole Ion Trap. Anal. Chem. 82, 5686–5696. https://doi.org/10.1021/ac100703w (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Cataldi, T. R. I., Rubino, A., Lelario, F. & Bufo, S. A. Naturally occuring glucosinolates in plant extracts of rocket salad (Eruca sativa L.) identified by liquid chromatography coupled with negative ion electrospray ionization and quadrupole ion-trap mass spectrometry. Rapid Commun. Mass Spectrom. 21, 2374–2388, doi:https://doi.org/10.1002/rcm.3101 (2007).Yang, Z. L., Kunert, G., Sporer, T., Kornig, J. & Beran, F. Glucosinolate abundance and composition in Brassicaceae influence sequestration in a specialist flea beetle. J. Chem. Ecol. 46, 186–197. https://doi.org/10.1007/s10886-020-01144-y (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Smirnoff, N. Ascorbic acid metabolism and functions: a comparison of plants and mammals. Free Radical Biol. and Medic. 122, 116–129. https://doi.org/10.1016/j.freeradbiomed.2018.03.033 (2018).CAS 
    Article 

    Google Scholar 
    Agerbirk, N., De Vos, M., Kim, J. H. & Jander, G. Indole glucosinolate breakdown and its biological effects. Phytochem. Rev. 8, 101–120. https://doi.org/10.1007/s11101-008-9098-0 (2009).CAS 
    Article 

    Google Scholar 
    Goggin, F. L., Avila, C. A. & Lorence, A. Vitamin C content in plants is modified by insects and influences susceptibility to herbivory. BioEssays 32, 777–790. https://doi.org/10.1002/bies.200900187 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kim, J. H., Lee, B. W., Schroeder, F. C. & Jander, G. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J. 54, 1015–1026 (2008).CAS 
    Article 

    Google Scholar 
    Liu, T. T. & Yang, T. S. Stability and antimicrobial activity of allyl isothiocyanate during long-term storage in an oil-in-water emulsion. J. Food Sci. 75, C445–C451. https://doi.org/10.1111/j.1750-3841.2010.01645.x (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Luang-In, V. & Rossiter, J. T. Stability studies of isothiocyanates and nitriles in aqueous media. Songklanakarin J. Sci. Technol. 37, 625–630 (2015).CAS 

    Google Scholar 
    Tsao, R., Yu, Q., Friesen, I., Potter, J. & Chiba, M. Factors affecting the dissolution and degradation of oriental mustard-derived sinigrin and allyl isothiocyanate in aqueous media. J. Agric. Food Chem. 48, 1898–1902. https://doi.org/10.1021/jf9906578 (2000).CAS 
    Article 
    PubMed 

    Google Scholar 
    Brodbeck, B. & Strong, D. in Insect Outbreaks (eds P. Barbosa & J. C. Schultz) Ch. 14, 347–363 (Academic Press, INC., 1987).Kumar, V. et al. Differential distribution of amino acids in plants. Amino Acids 49, 821–869. https://doi.org/10.1007/s00726-017-2401-x (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Millar, K. A., Gallagher, E., Burke, R., McCarthy, S. & Barry-Ryan, C. Proximate composition and anti-nutritional factors of fava-bean (Vicia faba), green-pea and yellow-pea (Pisum sativum) flour. J. Food Compos. Anal. 82, doi:https://doi.org/10.1016/j.jfca.2019.103233 (2019).Miller, R. W., McGrew, C., Wolff, I. A., Jones, Q. & Vanetten, C. H. Seed meal amino acids – amino acid composition of seed meals from 41 species of Cruciferae. J. Agric. Food Chem. 10, 426-430. https://doi.org/10.1021/jf60123a023 (1962).Article 

    Google Scholar 
    Fischer, W. N. et al. Low and high affinity amino acid H+-cotransporters for cellular import of neutral and charged amino acids. Plant J. 29, 717–731. https://doi.org/10.1046/j.1365-313X.2002.01248.x (2002).CAS 
    Article 
    PubMed 

    Google Scholar 
    Lea, P. J., Sodek, L., Parry, M. A. J., Shewry, R. & Halford, N. G. Asparagine in plants. Ann. Appl. Biol. 150, 1–26. https://doi.org/10.1111/j.1744-7348.2006.00104.x (2007).CAS 
    Article 

    Google Scholar 
    Leroy, P. D. et al. Aphid-host plant interactions: does aphid honeydew exactly reflect the host plant amino acid composition? Arthropod-Plant Inte. 5, 193–199. https://doi.org/10.1007/s11829-011-9128-5 (2011).Article 

    Google Scholar 
    Shukla, S. P. & Beran, F. Gut microbiota degrades toxic isothiocyanates in a flea beetle pest. Mol. Ecol. 29, 4692–4705. https://doi.org/10.1111/mec.15657 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Angelino, D. et al. Myrosinase-dependent and -independent formation and control of isothiocyanate products of glucosinolate hydrolysis. Front. Plant Sci. 6, 831. https://doi.org/10.3389/fpls.2015.00831 (2015).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liou, C. S. et al. A metabolic pathway for activation of dietary glucosinolates by a human gut symbiont. Cell 180, 717–729. https://doi.org/10.1016/j.cell.2020.01.023 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu, X. J. et al. Dietary broccoli alters rat cecal microbiota to improve glucoraphanin hydrolysis to bioactive isothiocyanates. Nutrients 9, 262. https://doi.org/10.3390/nu9030262 (2017).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    Sikorska-Zimny, K. & Beneduce, L. The metabolism of glucosinolates by gut microbiota. Nutrients 13, 2750. https://doi.org/10.3390/nu13082750 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Müller, C., Vogel, H. & Heckel, D. G. Transcriptional responses to short-term and long-term host plant experience and parasite load in an oligophagous beetle. Mol. Ecol. 26, 6370–6383. https://doi.org/10.1111/mec.14349 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    Rueckert, S., Betts, E. L. & Tsaousis, A. D. The symbiotic spectrum: where do the gregarines fit? Trends Parasitol. 35, 687–694. https://doi.org/10.1016/j.pt.2019.06.013 (2019).Article 
    PubMed 

    Google Scholar 
    Kühnle, A. & Müller, C. Responses of an oligophagous beetle species to rearing for several generations on alternative host plant species. Ecol. Entomol. 36, 125–134. https://doi.org/10.1111/j.1365-2311.2010.01256.x (2011).Article 

    Google Scholar 
    Sporer, T. et al. Hijacking the mustard-oil bomb: How a glucosinolate-sequestering flea beetle copes with plant myrosinases. Front. Plant Sci. 12, 645030. https://doi.org/10.3389/fpls.2021.645030 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kallenbach, M. et al. A robust, simple, high-throughput technique for time-resolved plant volatile analysis in field experiments. Plant J. 78, 1060–1072. https://doi.org/10.1111/tpj.12523 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kallenbach, M., Veit, D., Eilers, E. J. & Schuman, M. C. Application of silicone tubing for robust, simple, high-throughput, and time-resolved analysis of plant volatiles in field experiments. Bioprotocol 5, e1391 (2015).
    Google Scholar 
    Ruttkies, C., Schymanski, E. L., Wolf, S., Hollender, J. & Neumann, S. MetFrag relaunched: incorporating strategies beyond in silico fragmentation. J. Cheminf. 8, 3. https://doi.org/10.1186/s13321-016-0115-9 (2016).CAS 
    Article 

    Google Scholar 
    Kováts, E. Characterization of organic compounds by gas chromatography. Part 1. Retention indices of aliphatic halides, alcohols, aldehydes and ketones. Helv. Chim. Acta 41, 1915–1932, doi:https://doi.org/10.1002/hlca.19580410703 (1958).El-Sayed, A. M. The Pherobase: Database of Pheromones and Semiochemicals. (2012).McDanell, R., McLean, A. E. M., Hanley, A. B., Heaney, R. K. & Fenwick, G. R. Chemical and biological properties of indole glucosinolates (glucobrassicins): a review. Food Chem. Toxicol. 26, 59–70. https://doi.org/10.1016/0278-6915(88)90042-7 (1988).CAS 
    Article 
    PubMed 

    Google Scholar 
    Weber, G., Oswald, S. & Zöllner, U. Suitability of rapae cultivars with a different glucosinolate content for Brevicoryne brassicae (L) and Myzus persicae (Sulzer) (Hemiptera, Aphididae). Z. Pflanzenk. Pflanzenschutz 93, 113–124 (1986).CAS 

    Google Scholar 
    Wadleigh, R. W. & Yu, S. J. Detoxification of isothiocynante allelochemicals by glutathione transferase in three lepidopterous species. J. Chem. Ecol. 14, 1279–1288. https://doi.org/10.1007/bf01019352 (1988).CAS 
    Article 
    PubMed 

    Google Scholar 
    Francis, F., Lognay, G., Wathelet, J. P. & Haubruge, E. Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata. J. Chem. Ecol. 27, 243–256. https://doi.org/10.1023/A:1005672220342 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    Aliabadi, A., Renwick, J. A. A. & Whitman, D. W. Sequestration of glucosinolates by harlequin bug Murgantia histrionica. J. Chem. Ecol. 28, 1749–1762. https://doi.org/10.1023/a:1020505016637 (2002).CAS 
    Article 
    PubMed 

    Google Scholar 
    Bridges, M. et al. Spatial organization of the glucosinolate-myrosinase system in brassica specialist aphids is similar to that of the host plant. Proc. R. Soc. B-Biol. Sci. 269, 187–191. https://doi.org/10.1098/rspb.2001.1861 (2002).CAS 
    Article 

    Google Scholar 
    Müller, C., Agerbirk, N. & Olsen, C. E. Lack of sequestration of host plant glucosinolates in Pieris rapae and P. brassicae. Chemoecology 13, 47–54, doi: https://doi.org/10.1007/s000490300005 (2003).Francis, F., Vanhaelen, N. & Haubruge, E. Glutathione S-transferases in the adaptation to plant secondary metabolites in the Myzus persicae aphid. Arch. Insect Biochem. Physiol. 58, 166–174. https://doi.org/10.1002/arch.20049 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Müller, C. & Wittstock, U. Uptake and turn-over of glucosinolates sequestered in the sawfly Athalia rosae. Insect Biochem. Mol. Biol. 35, 1189–1198. https://doi.org/10.1016/j.ibmb.2005.06.001 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    Agerbirk, N., Müller, C., Olsen, C. E. & Chew, F. S. A common pathway for metabolism of 4-hydroxybenzylglucosinolate in Pieris and Anthocaris (Lepidoptera: Pieridae). Biochem. Syst. Ecol. 34, 189–198. https://doi.org/10.1016/j.bse.2005.09.005 (2006).CAS 
    Article 

    Google Scholar 
    Vergara, F. et al. Glycine conjugates in a lepidopteran insect herbivore: the metabolism of benzylglucosinolate in the cabbage white butterfly Pieris rapae. ChemBioChem 7, 1982–1989. https://doi.org/10.1002/cbic.200600280 (2006).Article 
    PubMed 

    Google Scholar 
    Agerbirk, N., Olsen, C. E., Topbjerg, H. B. & Sørensen, J. C. Host plant-dependent metabolism of 4-hydroxybenzylglucosinolate in Pieris rapae: Substrate specificity and effects of genetic modification and plant nitrile hydratase. Insect Biochem. Mol. Biol. 37, 1119–1130. https://doi.org/10.1016/j.ibmb.2007.06.009 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    Kazana, E. et al. The cabbage aphid: a walking mustard oil bomb. Proc. R. Soc. B-Biol. Sci. 274, 2271–2277 (2007).CAS 
    Article 

    Google Scholar 
    Agerbirk, N., Olsen, C. E., Poulsen, E., Jacobsen, N. & Hansen, P. R. Complex metabolism of aromatic glucosinolates in Pieris rapae caterpillars involving nitrile formation, hydroxylation, demethylation, sulfation, and host plant dependent carboxylic acid formation. Insect Biochem. Mol. Biol. 40, 126–137. https://doi.org/10.1016/j.ibmb.2010.01.003 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Opitz, S. E. W., Jensen, S. R. & Muller, C. Sequestration of glucosinolates and iridoid glucosides in sawfly species of the genus Athalia and their role in defense against ants. J. Chem. Ecol. 36, 148–157. https://doi.org/10.1007/s10886-010-9740-3 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Opitz, S. E. W., Mix, A., Winde, I. B. & Müller, C. Desulfation followed by sulfation: metabolism of benzylglucosinolate in Athalia rosae (Hymenoptera: Tenthredinidae). ChemBioChem 12, 1252–1257. https://doi.org/10.1002/cbic.201100053 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    Elbaz, M. et al. Asymmetric adaptation to indolic and aliphatic glucosinolates in the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae). Mol. Ecol. 21, 4533–4546. https://doi.org/10.1111/j.1365-294X.2012.05713.x (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Opitz, S. E. W. et al. Host shifts from Lamiales to Brassicaceae in the sawfly genus Athalia. PLoS ONE 7, e33649. https://doi.org/10.1371/journal.pone.0033649 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Stauber, E. J. et al. Turning the “Mustard oil bomb” into a “Cyanide bomb”: aromatic glucosinolate metabolism in a specialist insect herbivore. PLoS ONE 7, e35545. https://doi.org/10.1371/journal.pone.0035545 (2012).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gloss, A. D. et al. Evolution in an ancient detoxification pathway is coupled with a transition to herbivory in the Drosophilidae. Mol. Biol. Evol. 31, 2441–2456. https://doi.org/10.1093/molbev/msu201 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Goodey, N. A., Florance, H. V., Smirnoff, N. & Hodgson, D. J. Aphids pick their poison: selective sequestration of plant chemicals affects host plant use in a specialist herbivore. J. Chem. Ecol. 41, 956–964. https://doi.org/10.1007/s10886-015-0634-2 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Jeschke, V. et al. How glucosinolates affect generalist lepidopteran larvae: growth, development and glucosinolate metabolism. Front. Plant Sci. 8, doi:https://doi.org/10.3389/fpls.2017.01995 (2017).Steiner, A. M., Busching, C., Vogel, H. & Wittstock, U. Molecular identification and characterization of rhodaneses from the insect herbivore Pieris rapae. Sci. Rep. 8, 10819. https://doi.org/10.1038/s41598-018-29148-5 (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ahn, S. J. et al. Identification and evolution of glucosinolate sulfatases in a specialist flea beetle. Sci. Rep. 9, 15725. https://doi.org/10.1038/s41598-019-51749-x (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Malka, O. et al. Glucosylation prevents plant defense activation in phloem-feeding insects. Nat. Chem. Biol. 16, 1420–1426. https://doi.org/10.1038/s41589-020-00658-6 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Sun, R. et al. Detoxification of plant defensive glucosinolates by an herbivorous caterpillar is beneficial to its endoparasitic wasp. Mol. Ecol. 29, 4014–4031. https://doi.org/10.1111/mec.15613 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Manivannan, A. et al. Identification of a sulfatase that detoxifies glucosinolates in the phloem-feeding insect Bemisia tabaci and prefers indolic glucosinolates. Front. Plant Sci. 12, 671286. https://doi.org/10.3389/fpls.2021.671286 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yang, Z. L. et al. Sugar transporters enable a leaf beetle to accumulate plant defense compounds. Nat. Commun. 12, 2658. https://doi.org/10.1038/s41467-021-22982-8 (2021).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Reply to: “Steller’s sea cow uncertain history illustrates importance of ecological context when interpreting demographic histories from genomes”

    Sharko, F. S. et al. Steller’s sea cow genome suggests this species began going extinct before the arrival of Paleolithic humans. Nat. Commun. 12, 2215 (2021).ADS 
    CAS 
    Article 

    Google Scholar 
    Crerar, L. D., Crerar, A. P., Domning, D. P. & Parsons, E. C. Rewriting the history of an extinction-was a population of Steller’s sea cows (Hydrodamalis gigas) at St Lawrence Island also driven to extinction? Biol. Lett. 10, 20140878 (2014).Article 

    Google Scholar 
    Domning, D. P., Thomason, J. & Corbett, D. G. Steller’s sea cow in the Aleutian Islands. Mar. Mamm. Sci. 23, 976–983 (2007).Article 

    Google Scholar 
    Savinetsky, A. B., Kiseleva, N. K. & Khassanov, B. F. Dynamics of sea mammal and bird populations of the Bering Sea region over the last several millennia. Palaeogeogra. Palaeoclimatol. Palaeoecol. 20, 335–352 (2004).ADS 
    Article 

    Google Scholar 
    Whitmore, F. C. & Gard, L. M. J. Steller’s sea cow (Hydrodamalis gigas) of late Pleistocene age from Amchitka, Aleutian Islands, Alaska. US Geol. Surv. Prof. Pap. 1036, 1–19 (1977).
    Google Scholar 
    Sheppard, J. K. et al. Movement heterogeneity of dugongs, Dugong dugon (Muller), over large spatial scales. J. Exp. Mar. Biol. Ecol. 334, 64–83 (2006).Article 

    Google Scholar 
    Deutsch C. J., et al. Seasonal movements, migratory behavior, and site fidelity of West Indian manatees along the Atlantic Coast of the United States. Wildlife Monogr., 151, 1–77 (2003).Reed, R. K. Transport of the Alaskan Stream. Nature 220, 681–682 (1968).ADS 
    Article 

    Google Scholar 
    Detlef, H. et al. Sea ice dynamics across the Mid-Pleistocene transition in the Bering Sea. Nat. Commun. 9, 941 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    Ragen, T. J., Antonelis, G. A. & Kiyota, M. Early migration of northern fur-seal pups from St-Paul Island, Alaska. J. Mammal. 76, 1137–1148 (1995).Article 

    Google Scholar 
    Estes, J. A., Burdin, A. & Doak, D. F. Sea otters, kelp forests, and the extinction of Steller’s sea cow. Proc. Natl Acad. Sci. USA 113, 880–885 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    Larson, S., Jameson, R., Etnier, M., Jones, T. & Hall, R. Genetic diversity and population parameters of sea otters, Enhydra lutris, before fur trade extirpation from 1741–1911. PLoS ONE 7, e32205 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    Bullen, C. D., Campos, A. A., Gregr, E. J., McKechnie, I. & Chan, K. M. A. The ghost of a giant – Six hypotheses for how an extinct megaherbivore structured kelp forests across the North Pacific Rim. Glob. Ecol. Biogeogr. 30, 2101–2118 (2021).Article 

    Google Scholar 
    Plon, S., Thakur, V., Parr, L. & Lavery, S. D. Phylogeography of the dugong (Dugong dugon) based on historical samples identifies vulnerable Indian Ocean populations. PLoS ONE 14, e0219350 (2019).CAS 
    Article 

    Google Scholar 
    Seddon, J. M. et al. Fine scale population structure of dugongs (Dugong dugon) implies low gene flow along the southern Queensland coastline. Conserv. Genet. 15, 1381–1392 (2014).Article 

    Google Scholar 
    Clark, P. U. et al. The last glacial maximum. Science 325, 710–714 (2009).ADS 
    CAS 
    Article 

    Google Scholar  More

  • in

    Value wild animals’ carbon services to fill the biodiversity financing gap

    Pettorelli, N. et al. J. Appl. Ecol. 58, 2384–2393 (2021).Article 

    Google Scholar 
    CBD High-Level Panel Resourcing the Aichi Biodiversity Targets: An Assessment of Benefits, Investments and Resource Needs for Implementing the Strategic Plan for Biodiversity 2011–2020 (Secretariat of the Convention on Biological Diversity, 2014).Schmitz, O. J. et al. Science 362, eaar3213 (2018).Article 

    Google Scholar 
    Krause, T. & Nielsen, M. R. Forests 10, 344 (2019).Article 

    Google Scholar 
    Jørgensen, D. BioScience 63, 719–720 (2013).Article 

    Google Scholar 
    Berzaghi, F., Chami, R., Cosimano, T. & Fullenkamp, C. Proc. Natl Acad. Sci. USA 119, e2120426119 (2022).Article 

    Google Scholar 
    van Duuren, E., Plantinga, A. & Scholtens, B. J. Bus. Ethics 138, 525–533 (2016).Article 

    Google Scholar 
    Broadstock, D. C., Chan, K., Cheng, L. T. W. & Wang, X. Finance Res. Lett. 38, 101716 (2021).Article 

    Google Scholar 
    Joos, F., Meyer, R., Bruno, M. & Leuenberger, M. Geophys. Res. Lett. 26, 1437–1440 (1999).CAS 
    Article 

    Google Scholar 
    Wang, F. et al. Biol. Conserv. 253, 108913 (2021).Article 

    Google Scholar 
    Sullivan, S. Antipode 45, 198–217 (2013).Article 

    Google Scholar 
    Kamilaris, A., Cole, I. R. & Prenafeta-Boldú, F. X., in Food Technology Disruptions (ed. Galanakis, C. M.) 247–284 (Academic Press, 2021).O’Donnell, E. & Talbot-Jones, J. Ecol. Soc. 23, 7 (2018).Article 

    Google Scholar 
    Anderson, K. & Peters, G. Science 354, 182–183 (2016).CAS 
    Article 

    Google Scholar 
    Berzaghi, F. et al. Nat. Geosci. 12, 725–729 (2019).CAS 
    Article 

    Google Scholar 
    Mariani, G. et al. Sci. Adv. 6, eabb4848 (2020).CAS 
    Article 

    Google Scholar 
    Martin, A. H., Pearson, H. C., Saba, G. K. & Olsen, E. M. One Earth 4, 680–693 (2021).Article 

    Google Scholar 
    Durfort, A., Mariani, G., Troussellier, M., Tulloch, V. & Mouillot, D. Preprint at Research Square https://doi.org/10.21203/rs.3.rs-92037/v1 (2021).Norris, K., Terry, A., Hansford, J. P. & Turvey, S. T. Trends Ecol. Evol. 35, 919–926 (2020).Article 

    Google Scholar 
    Berzaghi, F. et al. Ecography 41, 1934–1954 (2018).Article 

    Google Scholar  More

  • in

    Regenerative living cities and the urban climate–biodiversity–wellbeing nexus

    CIAT Global Rural-Urban Mapping Project, v1 (GRUMPv1): Urban Extents Grid (NASA SEDAC, 2011).Global Status Report for Buildings and Construction: Towards a Zero-Emission, Efficient and Resilient Buildings and Construction Sector (UNEP, 2020).Harris, N. L. et al. Nat. Clim. Change 11, 234–240 (2021).Article 

    Google Scholar 
    Reid, W. V. et al. Ecosystems and Human Well-being: Biodiversity Synthesis (Millenium Ecosystem Assessment, World Resources Institute, 2005).Xu, C. et al. Resour. Conserv. Recycl. 151, 104478 (2019).Article 

    Google Scholar 
    Su, J., Friess, D. A. & Gasparatos, A. Nat. Commun. 12, 5050 (2021).CAS 
    Article 

    Google Scholar 
    van den Berg, M. et al. Urban For. Urban Green. 14, 806–816 (2015).Article 

    Google Scholar 
    Aerts, R., Honnay, O. & Van Nieuwenhuyse, A. Br. Med. Bull. 127, 5–22 (2018).Article 

    Google Scholar 
    Lindenmayer, D. et al. Ecol. Lett. 11, 78–91 (2008).
    Google Scholar 
    Knapp, S., Jaganmohan, M. & Schwarz, N. in Atlas of Ecosystem Services: Drivers, Risks, and Societal Responses (eds Schröter, M. et al.) 167–172 (Springer, 2019).Kim, H. Y. Geomat. Nat. Hazards Risk 12, 1181–1194 (2021).Article 

    Google Scholar 
    Vargas-Hernández, J. G., Pallagst, K. & Zdunek-Wielgołaska, J. in Handbook of Engaged Sustainability (ed. Marques, J.) 885–916 (Springer, 2018).Manso, M. et al. Renew. Sustain. Energy Rev. 135, 110111 (2021).Article 

    Google Scholar 
    Assimakopoulos, M.-N. et al. Sustainability 12, 3772 (2020).CAS 
    Article 

    Google Scholar 
    Mora-Melià, D. et al. Sustainability 10, 1130 (2018).Article 

    Google Scholar 
    IPBES. Curr. Opin. Environ. Sustain. 26, 7–16 (2017).
    Google Scholar 
    Schröpfer, T. & Menz, S. in Dense and Green Building Typologies: Research, Policy and Practice Perspectives (eds Schröpfer, T. & Menz, S.) 1–4 (Springer, 2019).Pedersen Zari, M. & Hecht, K. Biomimetics 5, 18 (2020).Article 

    Google Scholar  More

  • in

    Accounting for ecosystem service values in climate policy

    IPCC Climate Change 2007: Synthesis Report (eds Pachauri, R. K. & Reisinger, A.) (IPCC, 2007).Boyd, J. & Banzhaf, S. Ecol. Econ. 63, 616–626 (2007).Article 

    Google Scholar 
    Ruhl, J. B. et al. Front. Ecol. Environ. 19, 519–525 (2021).Article 

    Google Scholar 
    Carleton, T. & Greenstone, M. Updating the United States Government’s Social Cost of Carbon Working Paper 2021-04 (Univ. Chicago, Becker Friedman Institute for Economics, 2021).Mandle, L. et al. Nat. Sustain. 4, 161–169 (2021).Article 

    Google Scholar 
    Druckenmiller, H. Estimating an Economic and Social Value of Forests: Evidence from Tree Mortality in the American West (Univ. California Berkeley, 2021).Burkett, V. R. et al. Ecol. Complexity 2, 357–394 (2005).Article 

    Google Scholar 
    Hanley, N. & Czajkowski, M. Rev. Environ. Econ. Policy 13, 248–266 (2019).Article 

    Google Scholar 
    Mendelsohn, R. Rev. Environ. Econ. Policy 13, 267–282 (2019).Article 

    Google Scholar 
    Fenichel, E. P. et al. Proc. Natl Acad. Sci. USA 113, 2382–2387 (2016).CAS 
    Article 

    Google Scholar 
    Martin-Ortega, J. et al. Ecosyst. Serv. 50, 101327 (2021).Article 

    Google Scholar 
    Borrelli, P. et al. Proc. Natl Acad. Sci. USA 117, 21994–22001 (2020).CAS 
    Article 

    Google Scholar 
    Tropek, R. et al. Science 344, 981–981 (2014).CAS 
    Article 

    Google Scholar 
    Vardon, M., Burnett, P. & Dovers, S. Ecol. Econ. 124, 145–152 (2016).Article 

    Google Scholar 
    Bastien-Olvera, B. A. & Moore, F. C. Nat. Sustain. 4, 101–108 (2021).Article 

    Google Scholar 
    Beland, M. et al. For. Ecol. Manage. 450, 117484 (2019).Article 

    Google Scholar 
    Vargas, L., Willemen, L. & Hein, L. Environ. Manage. 63, 1–15 (2019).Article 

    Google Scholar 
    Hallgren, W. et al. Environ. Model. Softw. 76, 182–186 (2016).Article 

    Google Scholar 
    Rolf, E. et al. Nat. Commun. 12, 4392 (2021).CAS 
    Article 

    Google Scholar 
    Chernozhukov, V. et al. NBER Working Paper 24678 (National Bureau of Economic Research, 2018). More