Habitat-specificity in SAR11 is associated with a few genes under high selection.

The order Pelagibacterales (SAR11) is the most abundant group of heterotrophic bacteria in the global surface ocean, where individual sublineages likely play distinct roles in oceanic biogeochemical cycles. Yet, understanding the determinants of niche-partitioning within SAR11 has been a formidable challenge due to the high genetic diversity within individual SAR11 sublineages and the limited availability of high-quality genomes from both cultivation and metagenomic reconstruction. Through an integrated metapangenomic analysis of 71 new SAR11 isolate genomes and a time-series of metagenomes from the prominent source of isolation, we reveal an ecological and phylogenetic partitioning of metabolic traits across SAR11 genera. We resolve distinct habitat-preferences among genera for coastal or offshore environments of the tropical Pacific and identify a handful of genes involved in carbon and nitrogen metabolisms that appear to contribute to these contrasting lifestyles. Furthermore, we find that some habitat-specific genes experience high selective pressures, indicating that they are critical determinants of SAR11 fitness and niche differentiation. Together, these insights reveal the underlying evolutionary processes shaping niche-partitioning within sympatric and parapatric populations of SAR11 and demonstrate that the immense genomic diversity of SAR11 bacteria naturally segregates into ecologically and genetically cohesive units, or ecotypes, that vary in spatial distributions in the tropical Pacific.