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

Soil microbial diversity is often studied from the perspective of community composition, but less is known about genetic heterogeneity within species and how population structures are affected by dispersal, recombination, and selection. Genomic inferences about population structure can be 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 the population. Here we track genome-wide population genetic variation for 19 highly abundant bacterial species sampled from across a grassland meadow. Genomic nucleotide identity of assembled genomes was significantly associated with local geography for 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 specialized metabolite biosynthesis and extracellular transport were characterized by elevated genetic 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 site-specific differentiation of alleles, fewer recombinant events, and lower nucleotide diversity, suggesting recent selective sweeps for gene variants. Taken together, these results indicate that recombination and gene-specific selection commonly shape local soil bacterial genetic variation.