Abstract
Deeply sampled community genomic (metagenomic) datasets enable comprehensive analysis of heterogeneity in natural microbial populations. In this study, we used sequence data obtained from the dominant member of a low-diversity natural chemoautotrophic microbial community to determine how coexisting closely related individuals differ from each other in terms of gene sequence and gene content, and to uncover evidence of evolutionary processes that occur over short timescales. DNA sequence obtained from an acid mine drainage biofilm was reconstructed, taking into account the effects of strain variation, to generate a nearly complete genome tiling path for a Leptospirillum group II species closely related to L. ferriphilum (sampling depth ∼20×). The population is dominated by one sequence type, yet we detected evidence for relatively abundant variants (>99.5% sequence identity to the dominant type) at multiple loci, and a few rare variants. Blocks of other Leptospirillum group II types (∼94% sequence identity) have recombined into one or more variants. Variant blocks of both types are more numerous near the origin of replication. Heterogeneity in genetic potential within the population arises from localized variation in gene content, typically focused in integrated plasmid/phage-like regions. Some laterally transferred gene blocks encode physiologically important genes, including quorum-sensing genes of the LuxIR system. Overall, results suggest inter- and intrapopulation genetic exchange involving distinct parental genome types and implicate gain and loss of phage and plasmid genes in recent evolution of this Leptospirillum group II population. Population genetic analyses of single nucleotide polymorphisms indicate variation between closely related strains is not maintained by positive selection, suggesting that these regions do not represent adaptive differences between strains. Thus, the most likely explanation for the observed patterns of polymorphism is divergence of ancestral strains due to geographic isolation, followed by mixing and subsequent recombination.
Highlights
A characteristic of natural populations is that they are comprised of individuals that are, in the majority of cases, not genomically identical to each other
We address the question of whether adaptive differences between closely related, coexisting strains of Leptospirillum group II can be detected using population genetic analysis of single nucleotide polymorphisms (SNPs)
Population has given us both an unprecedented catalog of within-population variation and the opportunity to test hypotheses relating to the origin and maintenance of this variation
Summary
A characteristic of natural populations is that they are comprised of individuals that are, in the majority of cases, not genomically identical to each other. Heterogeneity present at any time reflects the outcome of the interplay between processes that create variation (e.g., mutation and lateral gene transfer) and those that remove it (e.g., selection and genetic drift). Variation between individuals appears both as divergence at the single nucleotide level and the presence of hypervariable gene ‘‘islands’’ within a more stable set of genes shared by multiple isolates [1,2,3,4]. The potential adaptive value of this variation is an important and controversial question in microbial ecology [5,6]. Through analyses of natural populations that explicitly consider genetic variability, it is possible to evaluate the basis for potential metabolic differences and infer aspects of the evolutionary processes that occur over relatively short timescales within natural communities
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