Homologous Recombination in Core Genomes Facilitates Marine Bacterial Adaptation

Acquisition of ecologically relevant genes is common among ocean bacteria, but whether it has a major impact on genome evolution in marine environments remains unknown. Here, we analyzed the core genomes of 16 phylogenetically diverse and ecologically relevant bacterioplankton lineages, each consisting of up to five genomes varying at the strain level. Statistical approaches identified from each lineage up to similar to 50 loci showing anomalously high divergence at synonymous sites, which is best explained by recombination with distantly related organisms. The enriched gene categories in these outlier loci match well with the characteristics previously identified as the key phenotypes of these lineages. Examples are antibiotic synthesis and detoxification in Phaeobacter inhibens, exopolysaccharide production in Alteromonas macleodii, hydrocarbon degradation in Marinobacter hydrocarbonoclasticus, and cold adaptation in Pseudo-alteromonas haloplanktis. Intriguingly, the outlier loci feature polysaccharide catabolism in Cellulophaga baltica but not in Cellulophaga lytica, consistent with their primary habitat preferences in macroalgae and beach sands, respectively. Likewise, analysis of Prochlorococcus showed that photosynthesis-related genes listed in the outlier loci are found only in the high-light-adapted ecotype and not in the low-light adapted ecotype. These observations strongly suggest that recombination with distant relatives is a key mechanism driving the ecological diversification among marine bacterial lineages. IMPORTANCE Acquisition of new metabolic genes has been known as an important mechanism driving bacterial evolution and adaptation in the ocean, but acquisition of novel alleles of existing genes and its potential ecological role have not been examined. Guided by population genetic theories, our genomic analysis showed that divergent allele acquisition is prevalent in phylogenetically diverse marine bacterial lineages and that the affected loci often encode metabolic functions that underlie the known ecological roles of the lineages under study.