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The bacterial orderMagnimaribacterales, previously known as the SAR86 lineage, is among the most abundant groups of planktonic bacteria inhabiting the global surface ocean. Despite their prevalence, our understanding of how this genetically diverse lineage partitions into units with coherent ecology and evolution remains limited. Here we surveyed multiple stations in the tropical Pacific Ocean using shotgun metagenomes and 16S rRNA gene amplicons to resolve distinct habitat preferences forMagnimaribacteraleslineages across nearshore, offshore, and open-ocean environments. The comprehensive collection of genomes that captured a large fraction of the known evolutionary breadth ofMagnimaribacterales, revealed patterns of ecotypic differentiation manifested primarily among genus-level clusters with specific clear preferences for distinct marine habitats. Enrichment analyses identified several functional genes associated with genomes from genera abundant in the nearshore environment, including those associated with sugar metabolism, peptide transport, and glycerophospholipid biosynthesis. Such metabolic adaptations likely facilitate the predominance of specificMagnimaribacteralesgenera in nearshore environments, promoting ecological partitioning across marine habitats. 

Abstract The orderPelagibacterales(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. Here, we take advantage of 71 new SAR11 genomes from strains we isolated from the tropical Pacific Ocean to evaluate the distribution of metabolic traits across thePelagibacteraceae,a recently classified family within the orderPelagibacteralesencompassing subgroups Ia and Ib. Our analyses of metagenomes generated from stations where the strains were isolated reveals distinct habitat preferences across SAR11 genera for coastal or offshore environments, and subtle but systematic differences in metabolic potential that support these observations. We also observe higher levels of selective forces acting on habitat-specific metabolic genes linked to SAR11 fitness and polyphyletic distributions of habitat preferences and metabolic traits across SAR11 genera, suggesting that contrasting lifestyles have emerged across multiple lineages independently. Together, these insights reveal 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. 

Abstract The bacterial orderPelagibacterales(SAR11) is among the most abundant and widely distributed microbial lineages across the global surface ocean, where it forms an integral component of the marine carbon cycle. However, the limited availability of high-quality genomes has hampered comprehensive insights into the ecology and evolutionary history of this critical group. Here, we increase the number of complete SAR11 isolate genomes fourfold by describing 81 new SAR11 strains from seven distinct lineages isolated from coastal and offshore surface seawater of the tropical Pacific Ocean. We leveraged comprehensive phylogenomic insights afforded by these isolates to characterize 24 monophyletic, discrete ecotypes with unique spatiotemporal patterns of distribution across the global ocean, which we define as genera. Our data illustrate fine-scale differentiation in patterns of detection with ecologically-relevant gene content variation for some closely related genomes, demonstrating instances of ecological speciation within SAR11 genera. Our study provides unique insight into complex environmental SAR11 populations, and proposes an ecology-informed hierarchy to pave a path forward for the systematic nomenclature for this clade. 

An integrated analysis framework shows a strong association between within-population genetic variation and protein structure.