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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.
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Ecophysiology and genomics of the brackish water adapted SAR11 subclade IIIa
Abstract The Order Pelagibacterales (SAR11) is the most abundant group of heterotrophic bacterioplankton in global oceans and comprises multiple subclades with unique spatiotemporal distributions. Subclade IIIa is the primary SAR11 group in brackish waters and shares a common ancestor with the dominant freshwater IIIb (LD12) subclade. Despite its dominance in brackish environments, subclade IIIa lacks systematic genomic or ecological studies. Here, we combine closed genomes from new IIIa isolates, new IIIa MAGS from San Francisco Bay (SFB), and 460 highly complete publicly available SAR11 genomes for the most comprehensive pangenomic study of subclade IIIa to date. Subclade IIIa represents a taxonomic family containing three genera (denoted as subgroups IIIa.1, IIIa.2, and IIIa.3) that had distinct ecological distributions related to salinity. The expansion of taxon selection within subclade IIIa also established previously noted metabolic differentiation in subclade IIIa compared to other SAR11 subclades such as glycine/serine prototrophy, mosaic glyoxylate shunt presence, and polyhydroxyalkanoate synthesis potential. Our analysis further shows metabolic flexibility among subgroups within IIIa. Additionally, we find that subclade IIIa.3 bridges the marine and freshwater clades based on its potential for compatible solute transport, iron utilization, and bicarbonate management potential. Pure culture experimentation validated differential salinity ranges in IIIa.1 and IIIa.3 and provided detailed IIIa cell size and volume data. This study is an important step forward for understanding the genomic, ecological, and physiological differentiation of subclade IIIa and the overall evolutionary history of SAR11.
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- Award ID(s):
- 1945279
- PAR ID:
- 10395257
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 17
- Issue:
- 4
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 620-629
- Size(s):
- p. 620-629
- Sponsoring Org:
- National Science Foundation
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