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Ecological Divergence with Gene Flow in a Thermophilic Cyanobacterium

  • Environmental Microbiology
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Abstract

How ecological diversity is maintained and distributed within populations is a longstanding question in microbial ecology. In the thermophilic cyanobacterium Synechococcus B′, high observed levels of recombination are predicted to maintain ecological variation despite the simultaneous action of diverse selective pressures on different regions of the genome. To investigate ecological diversity in these bacteria, we directly isolated laboratory strains of Synechococcus B′ from samples collected along the thermal gradients of two geothermal environments in Yellowstone National Park. Extensive recombination was evident for a multi-locus sequence data set, and, consequently, our sample did not exhibit the sequence clustering expected for distinct ecotypes evolving by periodic clonal selection. Evidence for local selective sweeps at specific loci suggests that sweeps may be common but that recombination is effective for maintaining diversity of unlinked genomic regions. Thermal performance for strain growth was positively associated with the temperature of the environment, indicating that Synechococcus B′ populations consist of locally adapted ecological specialists that occupy specific thermal niches. Because this ecological differentiation is observed despite the absence of dispersal barriers among sites, we conclude that these bacteria may freely exchange much of the genome but that barriers to gene flow exist for loci under direct temperature selection.

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References

  1. Cadillo-Quiroz H, Didelot X, Held NL, Herrera A, Darling A, Reno ML, Krause DJ, Whitaker RJ (2012) Patterns of gene flow define species of thermophilic Archaea. PLoS Biol. 10:e1001265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC, Szabó G, Polz MF, Alm EJ (2012) Population genomics of early events in the ecological differentiation of bacteria. Science 336:48–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ, Coe A, Ding H, Marttinen P, Malmstrom RR, Stocker R, Follows MJ, Stepanauskas R, Chisholm SW (2014) Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344:416–420

    Article  CAS  PubMed  Google Scholar 

  4. Kraemer SA, Boynton PJ (2017) Evidence for microbial local adaptation in nature. Mol. Ecol. 26:1860–1876

    Article  PubMed  Google Scholar 

  5. Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315:476–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cohan FM, Perry EB (2007) A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17:R373–R386

    Article  CAS  PubMed  Google Scholar 

  7. Wall CA, Koniges GJ, Miller SR (2014) Divergence with gene flow in a population of thermophilic bacteria: a potential role for spatially varying selection. Mol Ecol 23:3371–3383

    Article  PubMed  Google Scholar 

  8. Retchless AC, Lawrence JG (2007) Temporal fragmentation of speciation in bacteria. Science 317:1093–1096

    Article  CAS  PubMed  Google Scholar 

  9. Rosen MJ, Davison M, Bhaya D, Fisher DS (2015) Fine-scale diversity and extensive recombination in a quasisexual bacterial population occupying a broad niche. Science 348:1019–1023

    Article  CAS  PubMed  Google Scholar 

  10. Miller SR, Strong AL, Jones KL, Ungerer MC (2009) Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl Environ Microbiol 75:4565–4572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Haldane JBS (1948) The theory of a cline. J Genet 48:277–284

    Article  CAS  PubMed  Google Scholar 

  12. Endler J (1973) Differentiation of populations. Science 165:1228–1232

    Google Scholar 

  13. Wu C-I (2001) The genic view of the process of speciation. J Evol Biol 14:851–865

    Article  Google Scholar 

  14. Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Castenholz RW (1988) Culturing methods for cyanobacteria. Methods Enzymol 167:68–93

    Article  CAS  Google Scholar 

  16. Miller SR, Castenholz RW (2000) Evolution of thermotolerance in hot spring cyanobacteria of the genus Synechococcus. Appl Environ Microbiol 66:4222–4229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bhaya D, Grossman AR, Steunou A-S, Khuri N, Cohan FM, Hamamura N, Melendrez MC, Bateson MM, Ward DM, Heidelberg JF (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1:703–713

    Article  CAS  PubMed  Google Scholar 

  18. Inskeep WP, Jay ZJ, Tringe SG, Herrgård MJ, Rusch DB, YNP Metagenome Project Steering Committee and Working Group Members (2013) The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front Microbiol 4:67

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Klatt CG, Inskeep WP, Herrgard MJ, Jay ZJ, Rusch DB, Tringe SG, Parenteau MN, Ward DM, Boomer SM, Bryant DA, Miller SR (2013) Community structure and function of high-temperature chlorophototrophic microbial mats inhabiting diverse geothermal environments. Front Microbiol 4:106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Huson DH (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14(1):68–73

    Article  CAS  PubMed  Google Scholar 

  21. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  22. Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154

    Article  CAS  PubMed  Google Scholar 

  23. Huson DH, Bryant D (2005) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  24. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Allewalt JP, Bateson MM, Revsbech NP, Slack K, Ward DM (2006) Effect of temperature and light on growth of and photosynthesis by Synechococcus isolates typical of those predominating in the octopus spring microbial mat community of Yellowstone National Park. Appl Environ Microbiol 72:544–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ward DM, Castenholz RW, Miller SR (2012) Cyanobacteria in geothermal habitats. In: Whitton BE (ed) Ecology of cyanobacteria II. Springer, Dordrecht, pp 39–63

    Chapter  Google Scholar 

  27. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994

    Article  CAS  PubMed  Google Scholar 

  28. Humbert J-F, Barbe V, Latifi A, Gugger M, Calteau A, Coursin T, Lajus A, Castelli V, Oztas S, Samson G, Longin C, Medigue C, de Marsac NT (2013) A tribute to disorder in the genome of the bloom-forming freshwater cyanobacterium Microcystis aeruginosa. PLoS One 8:e70747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Meyer KA, Davis TW, Watson SB, Denef VJ, Berry MA, Dick GJ (2017) Genome sequences of lower Great Lakes Microcystis sp. reveal strain-specific genes that are present and expressed in western Lake Erie blooms. PLoS One 12:e0183859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Field work was conducted under National Park Service research permit YELL-5482. We thank two anonymous reviewers for comments on an earlier version of the manuscript.

Funding

This work was supported by National Science Foundation award EF-0801999 to SRM.

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Correspondence to Scott R. Miller.

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Miller, S.R., Carvey, D. Ecological Divergence with Gene Flow in a Thermophilic Cyanobacterium. Microb Ecol 78, 33–41 (2019). https://doi.org/10.1007/s00248-018-1267-0

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  • DOI: https://doi.org/10.1007/s00248-018-1267-0

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