Ecological Divergence with Gene Flow in a Thermophilic Cyanobacterium
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.
KeywordsDiversity Recombination Adaptation Selective sweep Thermophile
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.
This work was supported by National Science Foundation award EF-0801999 to SRM.
- 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 344:416–420CrossRefPubMedGoogle Scholar
- 12.Endler J (1973) Differentiation of populations. Science 165:1228–1232Google 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 4:67PubMedPubMedCentralGoogle 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 4:106CrossRefPubMedPubMedCentralGoogle 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 72:544–550CrossRefPubMedPubMedCentralGoogle 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:e70747CrossRefPubMedPubMedCentralGoogle Scholar