Host specificity of microbiome assembly and its fitness effects in phytoplankton

Abstract

Insights into symbiosis between eukaryotic hosts and their microbiomes have shifted paradigms on what determines host fitness, ecology, and behavior. Questions remain regarding the roles of host versus environment in shaping microbiomes, and how microbiome composition affects host fitness. Using a model system in ecology, phytoplankton, we tested whether microbiomes are host-specific, confer fitness benefits that are host-specific, and remain conserved in time in their composition and fitness effects. We used an experimental approach in which hosts were cleaned of bacteria and then exposed to bacterial communities from natural environments to permit recruitment of microbiomes. We found that phytoplankton microbiomes consisted of a subset of taxa recruited from these natural environments. Microbiome recruitment was host-specific, with host species explaining more variation in microbiome composition than environment. While microbiome composition shifted and then stabilized over time, host specificity remained for dozens of generations. Microbiomes increased host fitness, but these fitness effects were host-specific for only two of the five species. The shifts in microbiome composition over time amplified fitness benefits to the hosts. Overall, this work solidifies the importance of host factors in shaping microbiomes and elucidates the temporal dynamics of microbiome compositional and fitness effects.

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Fig. 1: Bacterial communities originating from three ponds in southeastern Michigan differed from the communities that migrated into jars containing initially axenic algae.
Fig. 2: Bacterial community composition described using a Bray–Curtis distance metric exhibited specificity to the algal-host species immediately following the 72-h incubation period of initially axenic algae in pond water.
Fig. 3: Relative to initial pond water, algal cultures were significantly under and over represented in numerous taxa (see Fig. S5 for results from all phyla).
Fig. 4: Five species of initially axenic algae inoculated with final phycospheres grew to significantly higher population densities than axenic algae inoculated with initial phycospheres.
Fig. 5: Phycosphere bacterial communities that assembled in association with five species of green eukaryotic algae were isolated and reintroduced to each of the five species of algae that had been rendered axenic.

References

  1. 1.

    Lau JA, Lennon JT. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci. 2012;109:14058.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  2. 2.

    Rosshart SP, Vassallo BG, Angeletti D, Hutchinson DS, Morgan AP, Takeda K, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. 2017;171:1015–1028.e13.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  3. 3.

    Lynch J, Hsiao E. Microbiomes as sources of emergent host phenotypes. Science. 2019;365:1405–9.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    Holland MA, Polacco JC. PPFMs and other covert contaminants: Is there more to plant physiology than just plant? Annu Rev Plant Physiol Plant Mol Biol. 1994;45:197–209.

    CAS  Article  Google Scholar 

  5. 5.

    Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13:260.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Coleman-Derr D, Tringe SG. Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance. Front Microbiol. 2014;5:283.

    PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Sampson TR, Mazmanian SK. Control of brain development, funtion, and behavior by the microbiome. Cell Host Microbe. 2015;17:565–76.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Siefert A, Zillig KW, Friesen ML, Strauss SY. Soil microbial communities alter conspecific and congeneric competition consistent with patterns of field coexistence in three Trifolium congeners. J Ecol. 2018;106:1876–91.

    CAS  Article  Google Scholar 

  9. 9.

    Siefert A, Zillig KW, Friesen ML, Strauss SY. Mutualists stabilize the coexistence of congeneric legumes. Am Naturalist. 2019;193:200–12.

    Article  Google Scholar 

  10. 10.

    Jackrel SL, Schmidt KC, Cardinale BJ, Denef VJ. Microbiomes reduce their host’s sensitivity to interspecific interactions. mBio. 2020;11:1–11.

    Article  Google Scholar 

  11. 11.

    Paustian K, Lehmann J, Ogle S, Reay D, Robertson GP, Smith P. Climate-smart soils. Nature. 2016;532:49.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  12. 12.

    Shi W, Moon CD, Leahy SC, Kang D, Froula J, Kittelmann S, et al. Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Genome Res. 2014;24:1517–25.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341:1241214.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  14. 14.

    Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, et al. The gut microbiome modulates colon tumorigenesis. mBio. 2013;4:e00692–13.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  15. 15.

    Kueneman JG, Woodhams DC, Harris R, Archer HM, Knight R, McKenzie VJ. Probiotic treatment restores protection against lethal fungal infection lost during amphibian captivity. Proc R Soc B: Biol Sci. 2016;283:20161553.

    Article  CAS  Google Scholar 

  16. 16.

    Cheng TL, Mayberry H, McGuire LP, Hoyt JR, Langwig KE, Nguyen H, et al. Efficacy of a probiotic bacterium to treat bats affected by the disease white‐nose syndrome. J Appl Ecol. 2017;54:701–8.

    Article  Google Scholar 

  17. 17.

    Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun. 2017;8:14213.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Björk JR, Hui FK, O’Hara RB, Montoya JM. Uncovering the drivers of host‐associated microbiota with joint species distribution modelling. Mol Ecol. 2018;27:2714–24.

    PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Youngblut ND, Reischer GH, Walters W, Schuster N, Walzer C, Stalder G, et al. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat Commun. 2019;10:2200.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  20. 20.

    David AS, Quintana-Ascencio PF, Menges ES, Thapa-Magar KB, Afkhami ME, Searcy CA. Soil microbiomes underlie population persistence of an endangered plant species. Am Naturalist. 2019;194:488–94.

    Article  Google Scholar 

  21. 21.

    David AS, Thapa‐Magar KB, Afkhami ME. Microbial mitigation–exacerbation continuum: a novel framework for microbiome effects on hosts in the face of stress. Ecology. 2018;99:517–23.

    PubMed  Article  PubMed Central  Google Scholar 

  22. 22.

    Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31:343–66.

    Article  Google Scholar 

  23. 23.

    Hutchinson GE. The paradox of the plankton. Am Naturalist. 1961;95:137–45.

    Article  Google Scholar 

  24. 24.

    Litchman E, Klausmeier CA, Schofield OM, Falkowski PG. The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett. 2007;10:1170–81.

    PubMed  Article  PubMed Central  Google Scholar 

  25. 25.

    Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, et al. The evolution of modern eukaryotic phytoplankton. Science. 2004;305:354.

    CAS  Article  Google Scholar 

  26. 26.

    Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science. 1998;281:237.

    CAS  Article  Google Scholar 

  27. 27.

    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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Kaczmarska I, Ehrman JM, Bates SS, Green DH, Léger C, Harris J. Diversity and distribution of epibiotic bacteria on Pseudo-nitzschia multiseries (Bacillariophyceae) in culture, and comparison with those on diatoms in native seawater. Harmful Algae. 2005;4:725–41.

    Article  Google Scholar 

  29. 29.

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30.

    Cirri E, Pohnert G. Algae–bacteria interactions that balance the planktonic microbiome. N Phytologist. 2019;223:100–6.

    Article  Google Scholar 

  31. 31.

    Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green JL. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci. 2014;111:13715–20.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  32. 32.

    Reveillaud J, Maignien L, Eren AM, Huber JA, Apprill A, Sogin ML, et al. Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J. 2014;8:1198–209.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Hird SM, Sánchez C, Carstens BC, Brumfield RT. Comparative gut microbiota of 59 neotropical bird species. Front Microbiol. 2015;6:1403.

    PubMed  PubMed Central  Article  Google Scholar 

  34. 34.

    Ochman H, Worobey M, Kuo C-H, Ndjango J-BN, Peeters M, Hahn BH, et al. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 2010;8:e1000546.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  35. 35.

    Moeller AH, Caro-Quintero A, Mjungu D, Georgiev AV, Lonsdorf EV, Muller MN, et al. Cospeciation of gut microbiota with hominids. Science. 2016;353:380.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. Human genetics shape the gut microbiome. Cell. 2014;159:789–99.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. 37.

    Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, et al. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci. 2013;110:6548.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. 38.

    Walters WA, Jin Z, Youngblut N, Wallace JG, Sutter J, Zhang W, et al. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc Natl Acad Sci. 2018;115:7368–73.

    PubMed  Article  PubMed Central  Google Scholar 

  39. 39.

    Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488:86.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Jackrel SL, White JD, Evans JT, Buffin K, Hayden K, Sarnelle O, et al. Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa. Mol Ecol. 2019;28:3994–4011.

  41. 41.

    Björk JR, Diéz-Vives C, Astudillo-García C, Archie EA, Montoya JM. Vertical transmission of sponge microbiota is inconsistent and unfaithful. Nat Ecol Evol. 2019;3:1172–83.

    PubMed  PubMed Central  Article  Google Scholar 

  42. 42.

    Wong AC-N, Luo Y, Jing X, Franzenburg S, Bost A, Douglas AE. The host as the driver of the microbiota in the gut and external environment of Drosophila melanogaster. Appl Environ Microbiol. 2015;81:6232–40.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Hird SM, Carstens BC, Cardiff SW, Dittmann DL, Brumfield RT. Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed Cowbird (Molothrus ater). PeerJ. 2014;2:e321.

    PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555:210–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  45. 45.

    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  Article  Google Scholar 

  46. 46.

    Eigemann F, Hilt S, Salka I, Grossart H-P. Bacterial community composition associated with freshwater algae: Species specificity vs. dependency on environmental conditions and source community. FEMS Microbiol Ecol. 2013;83:650–63.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  47. 47.

    Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T. Marine diatom species harbour distinct bacterial communities. Environ Microbiol. 2005;7:860–73.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  48. 48.

    Hold GL, Smith EA, Rappë MS, Maas EW, Moore ER, Stroempl C, et al. Characterisation of bacterial communities associated with toxic and non-toxic dinoflagellates: Alexandrium spp. and Scrippsiella trochoidea. FEMS Microbiol Ecol. 2001;37:161–73.

    CAS  Article  Google Scholar 

  49. 49.

    Krohn-Molt I, Alawi M, Förstner KU, Wiegandt A, Burkhardt L, Indenbirken D, et al. Insights into microalga and bacteria interactions of selected phycosphere biofilms using metagenomic, transcriptomic, and proteomic approaches. Front Microbiol. 2017;8:1941.

    PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    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. The ISME Journal. 2020.

  51. 51.

    Sapp M, Schwaderer AS, Wiltshire KH, Hoppe H-G, Gerdts G, Wichels A. Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol. 2007;53:683–99.

    PubMed  Article  PubMed Central  Google Scholar 

  52. 52.

    Schäfer H, Abbas B, Witte H, Muyzer G. Genetic diversity of ‘satellite’ bacteria present in cultures of marine diatoms. FEMS Microbiol Ecol. 2002;42:25–35.

    PubMed  PubMed Central  Google Scholar 

  53. 53.

    Sison-Mangus MP, Jiang S, Tran KN, Kudela RM. Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota. ISME J. 2014;8:63.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. 54.

    Dittami SM, Duboscq-Bidot L, Perennou M, Gobet A, Corre E, Boyen C, et al. Host–microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures. ISME J. 2016;10:51–63.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  55. 55.

    Schwab DB, Riggs HE, Newton ILG, Moczek AP. Developmental and ecological benefits of the maternally transmitted microbiota in a dung beetle. Am Naturalist. 2016;188:679–92.

    Article  Google Scholar 

  56. 56.

    Alexandrou MA, Cardinale BJ, Hall JD, Delwiche CF, Fritschie K, Narwani A, et al. Evolutionary relatedness does not predict competition and co-occurrence in natural or experimental communities of green algae. Proc R Soc B: Biol Sci. 2015;282:20141745.

    Article  Google Scholar 

  57. 57.

    Cho DH, Ramanan R, Kim BH, Lee J, Kim S, Yoo C, et al. Novel approach for the development of axenic microalgal cultures from environmental samples. J Phycol. 2013;49:802–10.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  58. 58.

    Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L. COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia. 1998;377:147–59.

    CAS  Article  Google Scholar 

  59. 59.

    Werner EE, McPeek MA. Direct and indirect effects of predators on two anuran species along an environmental gradient. Ecology. 1994;75:1368–82.

    Article  Google Scholar 

  60. 60.

    Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA, et al. The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem. 2011;43:1450–5.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. 61.

    Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. 62.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S. A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev. 2011;75:14–49.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–6.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  65. 65.

    Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. 66.

    McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS ONE. 2013;8:e61217.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  67. 67.

    Wickham H. ggplot2: elegant graphics for data analysis. Springer-Verlag New York; 2016.

  68. 68.

    Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009;26:139–40.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  69. 69.

    Sprouffske K, Wagner A. Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinform. 2016;17:172.

    Article  Google Scholar 

  70. 70.

    Vellend M The theory of ecological communities. Princeton University Press. 2016.

  71. 71.

    Vellend BM. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85:183–206.

    PubMed  Article  PubMed Central  Google Scholar 

  72. 72.

    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  Article  Google Scholar 

  73. 73.

    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  Article  Google Scholar 

  74. 74.

    Amin SA, Parker MS, Armbrust EV. Interactions between diatoms and bacteria. Microbiol Mol Biol Rev. 2012;76:667–84.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  75. 75.

    Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, et al. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci. 2003;100:1444–9.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  76. 76.

    Jasti S, Sieracki ME, Poulton NJ, Giewat MW, Rooney-Varga JN. Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Appl Environ Microbiol. 2005;71:3483–94.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    Sapp M, Wichels A, Gerdts G. Impacts of cultivation of marine diatoms on the associated bacterial community. Appl Environ Microbiol. 2007;73:3117–20.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. 78.

    Chisti Y. Biodiesel from microalgae. Biotechnol Adv. 2007;25:294–306.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  79. 79.

    Rosenberg JN, Kobayashi N, Barnes A, Noel EA, Betenbaugh MJ, Oyler GA. Comparative analyses of three Chlorella species in response to light and sugar reveal distinctive lipid accumulation patterns in the microalga C. sorokiniana. PloS ONE. 2014;9:e92460.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  80. 80.

    Morella NM, Weng FC-H, Joubert PM, Metcalf CJE, Lindow S, Koskella B. Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection. Proc Natl Acad Sci. 2020;117:1148–59.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  81. 81.

    Weiss P, Schweitzer B, Amann R, Simon M. Identification in situ and dynamics of bacteria on limnetic organic aggregates (lake snow). Appl Environ Microbiol. 1996;62:1998–2005.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  82. 82.

    Lemarchand C, Jardillier L, Carrias J-F, Richardot M, Debroas D, Sime-Ngando T, et al. Community composition and activity of prokaryotes associated to detrital particles in two contrasting lake ecosystems. FEMS Microbiol Ecol. 2006;57:442–51.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  83. 83.

    Ramanan R, Kang Z, Kim B-H, Cho D-H, Jin L, Oh H-M, et al. Phycosphere bacterial diversity in green algae reveals an apparent similarity across habitats. Algal Res. 2015;8:140–4.

    Article  Google Scholar 

  84. 84.

    Pernthaler J, Posch T, S̆imek K, Vrba J, Pernthaler A, Glöckner FO, et al. Predator-specific enrichment of Actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture. Appl Environ Microbiol. 2001;67:2145–55.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. 85.

    Šimek K, Kasalický V, Jezbera J, Jezberová J, Hejzlar J, Hahn MW. Broad habitat range of the phylogenetically narrow R-BT065 cluster, representing a core group of the Betaproteobacterial genus Limnohabitans. Appl Environ Microbiol. 2010;76:631–9.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  86. 86.

    Haukka K, Kolmonen E, Hyder R, Hietala J, Vakkilainen K, Kairesalo T, et al. Effect of nutrient loading on bacterioplankton community composition in lake mesocosms. Microb Ecol. 2006;51:137–46.

    PubMed  Article  PubMed Central  Google Scholar 

  87. 87.

    Kolmonen E, Sivonen K, Rapala J, Haukka K. Diversity of cyanobacteria and heterotrophic bacteria in cyanobacterial blooms in Lake Joutikas, Finland. Aquat Microb Ecol. 2004;36:201–11.

    Article  Google Scholar 

  88. 88.

    Schmidt ML, White JD, Denef VJ. Phylogenetic conservation of freshwater lake habitat preference varies between abundant bacterioplankton phyla. Environ Microbiol. 2016;18:1212–26.

    PubMed  Article  PubMed Central  Google Scholar 

  89. 89.

    Chiang E, Schmidt ML, Berry MA, Biddanda BA, Burtner A, Johengen TH, et al. Verrucomicrobia are prevalent in north-temperate freshwater lakes and display class-level preferences between lake habitats. PloS ONE. 2018;13:1–20.

    Google Scholar 

  90. 90.

    Simek K, Hornak K, Jezbera J, Nedoma J, Znachor P, Hejzlar J, et al. Spatio-temporal patterns of bacterioplankton production and community composition related to phytoplankton composition and protistan bacterivory in a dam reservoir. Aquat Microb Ecol. 2008;51:249–62.

    Article  Google Scholar 

  91. 91.

    Šimek K, Nedoma J, Znachor P, Kasalický V, Jezbera J, Hornňák K, et al. A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring. Limnol Oceanogr. 2014;59:1477–92.

    Article  CAS  Google Scholar 

  92. 92.

    Šimek K, Kasalický V, Zapomělová E, Horňák K. Alga-derived substrates select for distinct Betaproteobacterial lineages and contribute to niche separation in Limnohabitans strains. Appl Environ Microbiol. 2011;77:7307–15.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  93. 93.

    Horňák K, Kasalický V, Šimek K, Grossart HP. Strain‐specific consumption and transformation of alga‐derived dissolved organic matter by members of the Limnohabitans‐C and Polynucleobacter‐B clusters of Betaproteobacteria. Environ Microbiol. 2017;19:4519–35.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  94. 94.

    Spaink HP. Root nodulation and infection factors produced by Rhizobial bacteria. Annu Rev Microbiol. 2000;54:257–88.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  95. 95.

    Pérez‐Pantoja D, Donoso R, Agulló L, Córdova M, Seeger M, Pieper DH, et al. Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol. 2012;14:1091–117.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  96. 96.

    Denef VJ, Carrick HJ, Cavaletto J, Chiang E, Johengen TH, Vanderploeg HA. Lake bacterial assemblage composition is sensitive to biological disturbance caused by an invasive filter feeder. mSphere. 2017;2:e00189-17.

    PubMed  PubMed Central  Article  Google Scholar 

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Acknowledgements

We thank Dylan Baker, James Lauer, Anna Ortega, and Nate Arringdale for assistance with processing samples. We thank Prof. Brad J. Cardinale (BJC) for contributing algal cultures and facilities, Ruben Props for optimization of the TaxAss/mothur SOP, and Jacob Evans for assistance with data analysis. We also thank participating undergraduate students of the 2018 M-Sci summer class cohort for assisting with baseline experiments. This work was funded by an NSF-EAGER #1737680 to VJD, EFRI-PRSB #1332342 to VJD and BJC, and a Dow Sustainability Postdoctoral Fellowship to SLJ.

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VJD and SLJ conceived of project design, SLJ carried out phycosphere assembly experiment and phycosphere swap experiment, JWY extracted 16S rRNA DNA and analyzed these data, KCS rendered algae axenic and contributed to project design, SLJ and VJD drafted the paper with contributions from all other authors.

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Correspondence to Sara L. Jackrel or Vincent J. Denef.

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Jackrel, S.L., Yang, J.W., Schmidt, K.C. et al. Host specificity of microbiome assembly and its fitness effects in phytoplankton. ISME J (2020). https://doi.org/10.1038/s41396-020-00812-x

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