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Cryptic speciation of a pelagic Roseobacter population varying at a few thousand nucleotide sites

  • 1.

    Prgzelin BB, Alldredge AL. Primary production of marine snow during and after an upwelling event. Limnol Oceanogr. 1983;28:1156–67.

    Google Scholar 

  • 2.

    Shanks AL, Trent JD. Marine snow: microscale nutrient patches. Limnol Oceanogr. 1979;24:850–4.

    CAS  Google Scholar 

  • 3.

    Azam F, Malfatti F. Microbial structuring of marine ecosystems. Nat Rev Microbiol. 2007;5:782–91.

    CAS  PubMed  Google Scholar 

  • 4.

    Moran MA. The global ocean microbiome. Science. 2015;350:aac8455.

    PubMed  Google Scholar 

  • 5.

    Stocker R. Marine microbes see a sea of gradients. Science. 2012;338:628–33.

    CAS  PubMed  Google Scholar 

  • 6.

    Stocker R, Seymour JR, Samadani A, Hunt DE, Polz MF. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc Natl Acad Sci USA. 2008;105:4209–14.

    CAS  PubMed  Google Scholar 

  • 7.

    Stocker R, Seymour JR. Ecology and physics of bacterial chemotaxis in the ocean. Microbiol Mol Biol Rev. 2012;76:792–812.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 8.

    Rosenwasser S, Ziv C, Creveld SGvan, Vardi A. Virocell metabolism: metabolic innovations during host–virus interactions in the ocean. Trends Microbiol. 2016;24:821–32.

    CAS  PubMed  Google Scholar 

  • 9.

    Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet masters of the marine microbial realm. Nat Microbiol. 2018;3:754–66.

    CAS  PubMed  Google Scholar 

  • 10.

    Seymour JR, Amin SA, Raina J-B, Stocker R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol. 2017;2:1–12.

    Google Scholar 

  • 11.

    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  Google Scholar 

  • 12.

    Moran MA, Belas R, Schell MA, Gonzalez JM, Sun F, Sun S, et al. Ecological genomics of marine Roseobacters. Appl Environ Microbiol. 2007;73:4559–69.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 13.

    Bischoff V, Bunk B, Meier-Kolthoff JP, Spröer C, Poehlein A, Dogs M, et al. Cobaviruses—a new globally distributed phage group infecting Rhodobacteraceae in marine ecosystems. ISME J. 2019;13:1404–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 14.

    Zhan Y, Chen F. Bacteriophages that infect marine roseobacters: genomics and ecology. Environ Microbiol. 2019;21:1885–95.

    PubMed  Google Scholar 

  • 15.

    Ankrah NYD, May AL, Middleton JL, Jones DR, Hadden MK, Gooding JR, et al. Phage infection of an environmentally relevant marine bacterium alters host metabolism and lysate composition. ISME J. 2014;8:1089–100.

    CAS  PubMed  Google Scholar 

  • 16.

    Sonnenschein EC, Nielsen KF, D’Alvise P, Porsby CH, Melchiorsen J, Heilmann J, et al. Global occurrence and heterogeneity of the Roseobacter-clade species Ruegeria mobilis. ISME J. 2017;11:569–83.

    CAS  PubMed  Google Scholar 

  • 17.

    Luo H, Moran MA. Evolutionary ecology of the marine Roseobacter clade. Microbiol Mol Biol Rev. 2014;78:573–87.

    PubMed  PubMed Central  Google Scholar 

  • 18.

    Buchan A, LeCleir GR, Gulvik CA, González JM. Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol. 2014;12:686–98.

    CAS  PubMed  Google Scholar 

  • 19.

    Ramanan R, Kim B-H, Cho D-H, Oh H-M, Kim H-S. Algae–bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv. 2016;34:14–29.

    CAS  PubMed  Google Scholar 

  • 20.

    Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science. 2012;336:608–11.

    CAS  PubMed  Google Scholar 

  • 21.

    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 

  • 22.

    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 

  • 23.

    Green DH, Echavarri-Bravo V, Brennan D, Hart MC. Bacterial diversity associated with the coccolithophorid algae Emiliania huxleyi and Coccolithus pelagicus f. braarudii. BioMed Res Int. https://www.hindawi.com/journals/bmri/2015/194540/. Accessed 28 May 2020.

  • 24.

    González JM, Simó R, Massana R, Covert JS, Casamayor EO, Pedrós-Alió C, et al. Bacterial cmmunity structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl Environ Microbiol. 2000;66:4237–46.

    PubMed  PubMed Central  Google Scholar 

  • 25.

    Park BS, Guo R, Lim W-A, Ki J-S. Pyrosequencing reveals specific associations of bacterial clades Roseobacter and Flavobacterium with the harmful dinoflagellate Cochlodinium polykrikoides growing in culture. Mar Ecol. 2017;38:maec.12474.

    Google Scholar 

  • 26.

    Li S, Chen M, Chen Y, Tong J, Wang L, Xu Y, et al. Epibiotic bacterial community composition in red-tide dinoflagellate Akashiwo sanguinea culture under various growth conditions. FEMS Microbiol Ecol. 2019;95:fiz057.

    CAS  PubMed  Google Scholar 

  • 27.

    Bell W, Mitchell R. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull. 1972;143:265–77.

    Google Scholar 

  • 28.

    Cole JJ. Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst. 1982;13:291–314.

    Google Scholar 

  • 29.

    Moran MA, Buchan A, González JM, Heidelberg JF, Whitman WB, Kiene RP, et al. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature. 2004;432:910–3.

    CAS  PubMed  Google Scholar 

  • 30.

    Durham BP, Dearth SP, Sharma S, Amin SA, Smith CB, Campagna SR, et al. Recognition cascade and metabolite transfer in a marine bacteria-phytoplankton model system. Environ Microbiol. 2017;19:3500–13.

    CAS  PubMed  Google Scholar 

  • 31.

    Barak-Gavish N, Frada MJ, Ku C, Lee PA, DiTullio GR, Malitsky S, et al. Bacterial virulence against an oceanic bloom-forming phytoplankter is mediated by algal DMSP. Sci Adv. 2018;4:eaau5716.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 32.

    Segev E, Wyche TP, Kim KH, Petersen J, Ellebrandt C, Vlamakis H, et al. Dynamic metabolic exchange governs a marine algal-bacterial interaction. Elife. 2016;5:e17473.

    PubMed  PubMed Central  Google Scholar 

  • 33.

    Darling AE, Mau B, Perna NT. Progressivemauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE. 2010;5:e11147.

    PubMed  PubMed Central  Google Scholar 

  • 34.

    Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 35.

    Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol. 2015;11:e1004041.

    PubMed  PubMed Central  Google Scholar 

  • 36.

    Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet. 2012;8:e1002453.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 37.

    Sun Y, Luo H. Homologous recombination in core genomes facilitates marine bacterial adaptation. Appl Environ Microbiol. 2018;84:e02545–17.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 38.

    Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, et al. Population genomics of early events in the ecological differentiation of bacteria. Science. 2012;336:48–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 39.

    Achtman M. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol. 2008;62:53–70.

    CAS  PubMed  Google Scholar 

  • 40.

    Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, et al. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet. 2008;40:987–93.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 41.

    Morelli G, Song Y, Mazzoni CJ, Eppinger M, Roumagnac P, Wagner DM, et al. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat Genet. 2010;42:1140–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 42.

    Achtman M. Insights from genomic comparisons of genetically monomorphic bacterial pathogens. Philos Trans R Soc Lond B Biol Sci. 2012;367:860–7.

    PubMed  PubMed Central  Google Scholar 

  • 43.

    Didelot X, Maiden MCJ. Impact of recombination on bacterial evolution. Trends Microbiol. 2010;18:315–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 44.

    Vos M, Didelot X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 2009;3:199–208.

    CAS  PubMed  Google Scholar 

  • 45.

    Hanage WP. Not so simple after all: bacteria, their population genetics, and recombination. Cold Spring Harb Perspect Biol. 2016;8:a018069.

    PubMed  PubMed Central  Google Scholar 

  • 46.

    Fraser C, Hanage WP, Spratt BG. Recombination and the nature of bacterial speciation. Science. 2007;315:476–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 47.

    Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S, Homolka S, et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 2008;6:e311.

    PubMed  PubMed Central  Google Scholar 

  • 48.

    Holt KE, Baker S, Weill F-X, Holmes EC, Kitchen A, Yu J, et al. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet. 2012;44:1056–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 49.

    Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM, Al-Mashhadani MN, et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet. 2012;44:1215–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 50.

    Zhi X-Y, Zhao W, Li W-J, Zhao G-P. Prokaryotic systematics in the genomics era. Antonie Van Leeuwenhoek. 2012;101:21–34.

    PubMed  Google Scholar 

  • 51.

    Yahara K, Furuta Y, Oshima K, Yoshida M, Azuma T, Hattori M, et al. Chromosome painting in silico in a bacterial species reveals fine population structure. Mol Biol Evol. 2013;30:1454–64.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 52.

    Cadillo-Quiroz H, Didelot X, Held NL, Herrera A, Darling A, Reno ML, et al. Patterns of gene flow define species of thermophilic Archaea. PLoS Biol. 2012;10:e1001265.

  • 53.

    Ellegaard KM, Klasson L, Näslund K, Bourtzis K, Andersson SGE. Comparative genomics of Wolbachia and the bacterial species concept. PLoS Genet. 2013;9:e1003381.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 54.

    Wielgoss S, Didelot X, Chaudhuri RR, Liu X, Weedall GD, Velicer GJ, et al. A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus. ISME J. 2016;10:2468–77.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 55.

    Hoetzinger M, Hahn MW. Genomic divergence and cohesion in a species of pelagic freshwater bacteria. BMC Genom. 2017;18:794.

    Google Scholar 

  • 56.

    Arevalo P, VanInsberghe D, Elsherbini J, Gore J, Polz MF. A reverse ecology approach based on a biological definition of microbial populations. Cell. 2019;178:820–34.

    CAS  PubMed  Google Scholar 

  • 57.

    Bobay L-M, Ochman H. Biological species are universal across life’s domains. Genome Biol Evol. 2017;9:491–501.

    PubMed Central  Google Scholar 

  • 58.

    Engel P, Stepanauskas R, Moran NA. Hidden diversity in honey bee gut symbionts detected by single-cell genomics. PLoS Genet. 2014;10:e1004596.

    PubMed  PubMed Central  Google Scholar 

  • 59.

    Hughes AL, French JO. Homologous recombination and the pattern of nucleotide substitution in Ehrlichia ruminantium. Gene. 2007;387:31–7.

    CAS  PubMed  Google Scholar 

  • 60.

    Hughes AL, Friedman R. Nucleotide substitution and recombination at orthologous loci in Staphylococcus aureus. J Bacteriol. 2005;187:2698–704.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 61.

    Charrad M, Ghazzali N, Boiteau V, Niknafs A. NbClust: an R package for determining the relevant number of clusters in a data set. J Stat Softw. 2014;61:1–36.

    Google Scholar 

  • 62.

    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 

  • 63.

    Hünken M, Harder J, Kirst GO. Epiphytic bacteria on the Antarctic ice diatom Amphiprora kufferathii Manguin cleave hydrogen peroxide produced during algal photosynthesis. Plant Biol. 2008;10:519–26.

    PubMed  Google Scholar 

  • 64.

    Morris JJ, Kirkegaard R, Szul MJ, Johnson ZI, Zinser ER. Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by “helper” heterotrophic bacteria. Appl Environ Microbiol. 2008;74:4530–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 65.

    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 

  • 66.

    Cooper MB, Kazamia E, Helliwell KE, Kudahl UJ, Sayer A, Wheeler GL, et al. Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae. ISME J. 2019;13:334–45.

    CAS  PubMed  Google Scholar 

  • 67.

    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  Google Scholar 

  • 68.

    Helliwell KE. The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. New Phytol. 2017;216:62–8.

    CAS  PubMed  Google Scholar 

  • 69.

    Gao R, Krysciak D, Petersen K, Utpatel C, Knapp A, Schmeisser C, et al. Genome-wide RNA sequencing analysis of quorum sensing-controlled regulons in the plant-associated Burkholderia glumae PG1 strain. Appl Environ Microbiol. 2015;81:7993–8007.

    PubMed  PubMed Central  Google Scholar 

  • 70.

    Ng VH, Cox JS, Sousa AO, MacMicking JD, McKinney JD. Role of KatG catalase-peroxidase in mycobacterial pathogenesis: countering the phagocyte oxidative burst. Mol Microbiol. 2004;52:1291–302.

    CAS  PubMed  Google Scholar 

  • 71.

    Ivanova A, Miller C, Glinsky G, Eisenstark A. Role of rpoS (katF) in oxyR-independent regulation of hydroperoxidase I in Escherichia coli. Mol Microbiol. 1994;12:571–8.

    CAS  PubMed  Google Scholar 

  • 72.

    Amábile-Cuevas CF, Demple B. Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon. Nucleic Acids Res. 1991;19:4479–84.

    PubMed  PubMed Central  Google Scholar 

  • 73.

    Landfald B, Strøm AR. Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol. 1986;165:849–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 74.

    Lidbury I, Kimberley G, Scanlan DJ, Murrell JC, Chen Y. Comparative genomics and mutagenesis analyses of choline metabolism in the marine Roseobacter clade. Mol Microbiol. 2015;17:5048–62.

    CAS  Google Scholar 

  • 75.

    Bochner BR, Gadzinski P, Panomitros E. Phenotype microArrays for high-throughput phenotypic testing and assay of gene function. Genome Res. 2001;11:1246–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 76.

    Vaas LAI, Sikorski J, Hofner B, Fiebig A, Buddruhs N, Klenk H-P, et al. opm: an R package for analysing OmniLog(R) phenotype microarray data. Bioinformatics. 2013;29:1823–4.

    CAS  PubMed  Google Scholar 

  • 77.

    Mou X, Vila-Costa M, Sun S, Zhao W, Sharma S, Moran MA. Metatranscriptomic signature of exogenous polyamine utilization by coastal bacterioplankton. Environ Microbiol Rep. 2011;3:798–806.

    CAS  PubMed  Google Scholar 

  • 78.

    Porter SS, Chang PL, Conow CA, Dunham JP, Friesen ML. Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic. Mesorhizobium ISME J. 2017;11:248–62.

    CAS  PubMed  Google Scholar 

  • 79.

    Andam CP, Gogarten JP. Biased gene transfer in microbial evolution. Nat Rev Microbiol. 2011;9:543–55.

    CAS  PubMed  Google Scholar 

  • 80.

    Boucher Y, Cordero OX, Takemura A. Endemicity within global Vibrio cholerae populations. mBio. 2011;2:1–8.

    Google Scholar 

  • 81.

    Coleman ML, Chisholm SW. Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA. 2010;107:18634–9.

    CAS  PubMed  Google Scholar 

  • 82.

    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 

  • 83.

    Cordero OX, Polz MF. Explaining microbial genomic diversity in light of evolutionary ecology. Nat Rev Microbiol. 2014;12:263–73.

    CAS  PubMed  Google Scholar 

  • 84.

    Hoetzinger M, Schmidt J, Jezberová J, Koll U, Hahn MW. Microdiversification of a pelagic Polynucleobacter species Is mainly driven by acquisition of genomic islands from a partially interspecific gene pool. Appl Environ Microbiol. 2017;83:e02266–16.

    PubMed  PubMed Central  Google Scholar 

  • 85.

    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  Google Scholar 

  • 86.

    Christie-Oleza JA, Sousoni D, Lloyd M, Armengaud J, Scanlan DJ. Nutrient recycling facilitates long-term stability of marine microbial phototroph-heterotroph interactions. Nat Microbiol. 2017;2:17100.

    CAS  PubMed  PubMed Central  Google Scholar 


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