Evolutionary divergence and biogeography of sympatric niche-differentiated bacterial populations

Using multiple lines of evidence from denaturing gradient gel electrophoresis, environmental sequences and TaqMan quantitative PCR assays targeting a functional gene for sulfate respiration (dsr) affiliated with the geochemically important genus Desulfobulbus, we revealed strongly restricted distributions of specific genotypes and populations correlated with sampling position along an estuarine gradient free of dispersal barriers. Evidence of evolutionary divergence of populations was provided by three complementary analyses. First, analysis of molecular variance rejected the null hypothesis that genetic diversity within each sampling site was not significantly different than that of all sites pooled together (P<0.0001). Second, UniFrac and Parsimony tests showed phylogenetic clustering of sampling sites was highly significant (P<0.001). Third, pairwise F(ST) statistics showed significant evolutionary divergence of populations based on the location in the estuary. To test the hypothesis that environmental niche-driven evolutionary divergence can create and maintain microbial biogeography, we used both statistical inference and an experimental manipulation to assess the independent effects of environment and geography. Significant effects of each on genotype distributions and population divergence supported the hypothesis. Our data are consistent with both sympatric and parapatric models of speciation, and suggest niche partitioning can contribute to evolutionary divergence and observable biogeographic patterns in microbial communities even among closely related taxa at limited spatial scales without significant barriers to dispersal. The ISME Journal (2010) 4, 488-497; doi:10.1038/ismej.2009.146; published online 7 January 2010