Promiscuous and genome-wide recombination underlies the sequence-discrete species of the SAR11 lineage in the deep ocean

Surveys of microbial communities (metagenomics) or isolate genomes have revealed sequence-discrete species. That is, members of the same species show >95% average nucleotide identity (ANI) of shared genes among themselves vs. <83% ANI to members of other species while genome pairs showing between 83% and 95% ANI are comparatively rare. In these surveys, aquatic bacteria of the ubiquitous SAR11 clade (Class Alphaproteobacteria) are an outlier and often do not exhibit discrete species boundaries, suggesting the potential for alternate modes of genetic differentiation. To explore evolution in SAR11, we analyzed high-quality, single-cell amplified genomes, and companion metagenomes from an oxygen minimum zone in the Eastern Tropical Pacific Ocean, where the SAR11 make up ~20% of the total microbial community. Our results show that SAR11 do form several sequence-discrete species, but their ANI range of discreteness is shifted to lower identities between 86% and 91%, with intra-species ANI ranging between 91% and 100%. Measuring recent gene exchange among these genomes based on a recently developed methodology revealed higher frequency of homologous recombination within compared to between species that affects sequence evolution at least twice as much as diversifying point mutation across the genome. Recombination in SAR11 appears to be more promiscuous compared to other prokaryotic species, likely due to the deletion of universal genes involved in the mismatch repair, and has facilitated the spread of adaptive mutations within the species (gene sweeps), further promoting the high intraspecies diversity observed. Collectively, these results implicate rampant, genome-wide homologous recombination as the mechanism of cohesion for distinct SAR11 species.