Abstract
Despite extensive DNA sequencing data derived from natural microbial communities, it remains a major challenge to identify the key evolutionary and ecological forces that shape microbial populations. We have focused on the extensive microdiversity of the cyanobacterium Synechococcus sp., which is a dominant member of the dense phototrophic biofilms in the hot springs of Yellowstone National Park. From deep amplicon sequencing of many loci and statistical analyses of these data, we showed previously that the population has undergone an unexpectedly high degree of homologous recombination, unlinking synonymous SNP-pair correlations even on intragenic length scales. Here, we analyze the genic amino acid diversity, which provides new evidence of selection and insights into the evolutionary history of the population. Surprisingly, some features of the data, including the spectrum of distances between genic-alleles, appear consistent with primarily asexual neutral drift. Yet the non-synonymous site frequency spectrum has too large an excess of low-frequency polymorphisms to result from negative selection on deleterious mutations given the distribution of coalescent times that we infer. And our previous analyses showed that the population is not asexual. Taken together, these apparently contradictory data suggest that selection, epistasis, and hitchhiking all play essential roles in generating and stabilizing the diversity. We discuss these as well as potential roles of ecological niches at genomic and genic levels. From quantitative properties of the diversity and comparative genomic data, we infer aspects of the history and inter-spring dispersal of the meta-population since it was established in the Yellowstone Caldera. Our investigations illustrate the need for combining multiple types of sequencing data and quantitative statistical analyses to develop an understanding of microdiversity in natural microbial populations.
Highlights
Large-scale genetic surveys of microbes in complex environments continue to uncover a great deal of diversity at the species level and above
We focused on diversity within unicellular Synechococcus sp. communities residing in the microbial mats found in the effluent channels of Octopus Spring (OS) and Mushroom Spring (MS) in Yellowstone National Park (YNP), one of the best-studied populations of thermophilic cyanobacteria [15]
We begin with the 16S diversity, (3) finding that 92% of the sampled cyanobacterial population is within two single nucleotide polymorphisms (SNPs) ( 0.5% sequence divergence) of the Syn OS-B0 genome, but that alleles similar to Syn OS-A and even more diverged cyanobacterial subtypes are present at low levels
Summary
Large-scale genetic surveys of microbes in complex environments (e.g. the human microbiome [1], oceans [2], and soil [3]) continue to uncover a great deal of diversity at the species level and above. Other sequencing efforts have focused on microbial diversity among coexisting individuals within a single species Perhaps more surprisingly, these too tend to uncover rich, fine-scale genetic diversity or microdiversity (e.g. in microbiota of the human tongue [4], marine Prochlorococcus [5, 6] and Vibrio [7], and the thermophilic archaeon Sulfolobus islandicus [8]). These too tend to uncover rich, fine-scale genetic diversity or microdiversity (e.g. in microbiota of the human tongue [4], marine Prochlorococcus [5, 6] and Vibrio [7], and the thermophilic archaeon Sulfolobus islandicus [8]) Such diversity may be the product of ecological specialization to a multitude of finer scale niches, i.e. ecotypes [9]. Determining what mixture of ecological and evolutionary forces shapes microbial microdiversity in any particular context is a major challenge
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