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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. 

Abstract Islands in the tropical Pacific supply elevated nutrients to nearshore waters that enhance phytoplankton biomass and create hotspots of productivity in otherwise nutrient‐poor oceans. Despite the importance of these hotspots in supporting nearshore food webs, the spatial and temporal variability of phytoplankton enhancement and changes in the underlying phytoplankton communities across nearshore to open ocean systems remain poorly understood. In this study, a combination of flow cytometry, pigment analyses, 16S rRNA gene amplicons, and metagenomic sequencing provides a synoptic view of phytoplankton dynamics over a 4‐yr, near‐monthly time series across coastal Kāneʻohe Bay, Hawaiʻi, spanning from an estuarine Indigenous aquaculture system to the adjacent offshore environment. Through comparisons with measurements taken at Station ALOHA located in the oligotrophic North Pacific Subtropical Gyre, we observed a sharp and persistent transition between picocyanobacterial communities, fromSynechococcusclade II abundant in the nearshore toProchlorococcushigh‐light adapted clade II (HLII) proliferating in offshore and open ocean waters. In comparison to immediately adjacent offshore waters and the surrounding open ocean, phytoplankton biomass within Kāneʻohe Bay was dramatically elevated. Members of the phytoplankton community revealed strong seasonal patterns, while nearshore phytoplankton biomass positively correlated with wind speed, rainfall, and wind direction, and not water temperatures. These findings elucidate the spatiotemporal dynamics underlying transitions in ocean biogeochemistry and phytoplankton dynamics across estuarine to open ocean waters in the tropical Pacific and provide a foundation for quantifying deviations from baseline conditions due to ongoing climate change. 

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 SAR86 is one of the most abundant groups of bacteria in the global surface ocean. However, since its discovery over 30 years ago, it has remained recalcitrant to isolation and many details regarding this group are still unknown. Here, we report the cellular characteristics from the first SAR86 isolate brought into culture, Magnimaribacter mokuoloeensis strain HIMB1674, and use its closed genome in concert with over 700 environmental genomes to assess the phylogenomic and functional characteristics of this order-level lineage of marine Gammaproteobacteria. The SAR86 order Magnimaribacterales invests significant genomic resources into the capacity for $$\beta$$-oxidation, which is present in most genomes with high gene copy numbers. This cyclical set of reactions appears to be fed by components of cell membranes that include lipids such as phosphatidylcholine, phosphatidylethanolamine, glycolipids, and sulfolipids. In addition to the widespread capacity to degrade the side chain of steroidal compounds via $$\beta$$-oxidation, several SAR86 sublineages also appear able to fully degrade the steroid polycyclic ring structure as well as other aromatic, polycyclic, and heterocyclic molecules. Read recruitment from publicly available metagenomes reveals that the Magnimaribacterales compose up to 6% of the global surface ocean microbial community. Only a subset of genera drives these high relative abundances, with some more globally dominant and others restricted to specific oceanic regions. This study provides an unprecedented foundation through which to understand this highly abundant yet poorly understood lineage of marine bacteria and charts a path to bring more representatives of this order into laboratory culture. 

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. 

Islands in the tropical Pacific supply elevated nutrients to nearshore waters that enhance phytoplankton biomass and create hotspots of productivity in otherwise nutrient-poor oceans. Despite the importance of these hotspots in supporting nearshore food webs, the fine-scale spatial and temporal variability of phytoplankton enhancement and changes in the underlying phytoplankton communities across nearshore to open ocean systems remain poorly understood. In this study, a combination of flow cytometry, pigment analyses, 16S rRNA gene amplicons, and metagenomic sequencing provide a synoptic view of phytoplankton dynamics over a four-year, near-monthly time-series across coastal Kāneʻohe Bay, Hawaiʻi, spanning from an estuarine Indigenous aquaculture system to the adjacent offshore environment. Through comparisons with measurements taken at Station ALOHA located in the oligotrophic North Pacific Subtropical Gyre, we elucidated a sharp and persistent transition between picocyanobacterial communities, from Synechococcus abundant in the nearshore to Prochlorococcus proliferating in offshore and open ocean waters. In comparison to immediately adjacent offshore waters and the surrounding open ocean, phytoplankton biomass within Kānʻeohe Bay was dramatically elevated. While phytoplankton community composition revealed strong seasonal patterns, phytoplankton biomass positively correlated with wind speeds, rainfall, and wind direction, and not water temperatures. These findings reveal sharp transitions in ocean biogeochemistry and phytoplankton dynamics across estuarine to open ocean waters in the tropical Pacific and provide a foundation for quantifying deviations from baseline conditions due to ongoing climate change. 

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