Patterns of gene flow and divergence in natural populations of the thermophilic crenarchaeon Sulfolobus islandicus

What are the evolutionary forces that promote or constrain diversification of microbial species? I explored this question by investigating the population structure of the thermoacidophilic crenarchaeon Sulfolobus islandicus . One hundred forty Sulfolobus strains were isolated from five geothermal regions of Kamchatka, Russia; Western North America; and Iceland. Multilocus sequence analysis of these strains identifies five subpopulations that correspond to geographically isolated geothermal regions. Using a combination of phylogenetic and population genetic methods, I demonstrate that distribution of genetic diversity among subpopulations is consistent with a model of isolation by distance in which geographically isolated populations diverge due to low levels of gene flow between them. This evidence for geographic isolation challenges the widely accepted model of microbial biodiversity in which unrestricted dispersal constrains divergence in microbial species. Within a single population, I assessed the distribution of allelic diversity at six protein-coding loci among 60 individuals. Significant incongruence between gene geneologies and a lack of association between alleles provide evidence of frequent recombination among individuals. The persistence of recombinant genotypes in this population suggests a genetic structure that is not consistent with the predictions of the periodic selection model of evolution for clonally reproducing microorganisms. I discuss the ecological and evolutionary mechanisms that may maintain recombinant genotypes in the dynamic geothermal environment. Finally, multilocus sequence analyses of strains isolated for this study and two previously described Sulfolobus species identify a new species of Sulfolobus-Sulfolobus islandicus sp nov. Exploring fine-scale patterns of diversity along the continuum of genetic divergence from populations to species has identified fundamental evolutionary mechanisms that define the structure of diversity in thermoacidophilic Archaea.