Soil bacterial populations are shaped by recombination and gene-specific selection across a grassland meadow

Abstract

Soil microbial diversity is often studied from the perspective of community composition, but less is known about genetic heterogeneity within species. The relative impacts of clonal interference, gene-specific selection, and recombination in many abundant but rarely cultivated soil microbes remain unknown. Here we track genome-wide population genetic variation for 19 highly abundant bacterial species sampled from across a grassland meadow. Genomic inferences about population structure are made using the millions of sequencing reads that are assembled de novo into consensus genomes from metagenomes, as each read pair describes a short genomic sequence from a cell in each population. Genomic nucleotide identity of assembled genomes was significantly associated with local geography for over half of the populations studied, and for a majority of populations within-sample nucleotide diversity could often be as high as meadow-wide nucleotide diversity. Genes involved in metabolite biosynthesis and extracellular transport were characterized by elevated nucleotide diversity in multiple species. Microbial populations displayed varying degrees of homologous recombination and recombinant variants were often detected at 7-36% of loci genome-wide. Within multiple populations we identified genes with unusually high spatial differentiation of alleles, fewer recombinant events, elevated ratios of nonsynonymous to synonymous variants, and lower nucleotide diversity, suggesting recent selective sweeps for gene variants. Taken together, these results indicate that recombination and gene-specific selection commonly shape genetic variation in several understudied soil bacterial lineages.

Evolutionary ecology of natural comammox Nitrospira populations

“…3B). In general, recombination was lower in the waterworks populations than in populations inhabiting a grassland meadow 23 , where a similar study was conducted (Fig. 3B).…”

“…We also investigated local regions of the Nitrospira genomes with significantly higher FST values, as this is characteristic of local population-specific (here in each waterworks) selective pressures acting on specific loci 23 . Few loci were found with unusually high FST in some of the Nitrospira populations ( Supplementary Fig.…”

“…RSF2) (Supplementary Table 5). However, only two of these loci with unusually high site-specific differentiation of alleles (high FST) also had fewer recombinant events, and lower nucleotide diversity (Supplementary Table 5), which can be considered as a signal of recent selective sweep 23 . These results suggest that contrary to what it has been observed in several natural populations [23][24][25][26] , gene-specific sweeps seems to play a minor role in the evolution of Nitrospira spp.…”

“…3C). Purifying selection has frequently been observed in wild populations, and it was the case for populations inhabiting a grassland meadow 23 (pN/pS = 0.56 ± 0.17, n = 19), but this process seems to be especially strong in the waterworks populations (pN/pS = 0.34 ± 0.05, n = 24) (Two-Sample ttest, p < 0.0001) ( Fig. 3C), which suggests prior evolution to optimal adaptation to this stable environment, with purging of non-synonymous mutations.…”

“…Triplot composed of the nucleotide diversity, pN/pS ratio and D' values for the bacterial populations of this study (WW) as well as most abundant bacterial populations across grassland meadow 23 (Soil), and other Nitrospira populations abundant in other systems (Supplementary Table 6; CMX_FW, CMX_DWTP, NOB_DWTP, and CMX_Agric.Soil). Colour legends are displayed on the left of the figure.…”