Abstract
Members of the SAR11 order Pelagibacterales dominate the surface oceans. Their extensive diversity challenges emerging operational boundaries defined for microbial 'species' and complicates efforts of population genetics to study their evolution. Here, we employed single-amino acid variants (SAAVs) to investigate ecological and evolutionary forces that maintain the genomic heterogeneity within ubiquitous SAR11 populations we accessed through metagenomic read recruitment using a single isolate genome. Integrating amino acid and protein biochemistry with metagenomics revealed that systematic purifying selection against deleterious variants governs non-synonymous variation among very closely related populations of SAR11. SAAVs partitioned metagenomes into two main groups matching large-scale oceanic current temperatures, and six finer proteotypes that connect distant oceanic regions. These findings suggest that environmentally-mediated selection plays a critical role in the journey of cosmopolitan surface ocean microbial populations, and the idea 'everything is everywhere but the environment selects' has credence even at the finest resolutions.
Highlights
The SAR11 family Pelagibacteraceae [1] represents the most ubiquitous free-living lineage of heterotrophic bacteria in the world’s oceans [2, 3, 4, 5, 6, 7]
We developed a novel approach to characterize single-amino acid variants (SAAVs) from metagenomic data and investigated evolutionary dynamics operating on SAR11 Low-Latitude Population A’ (S-LLPA)
We characterized the relative abundances of 21 SAR11 isolates across four oceans and two seas using a dataset of 103 metagenomes, including 93 samples from the TARA Oceans Project [17] and 10 samples from the Ocean Sampling Day Project [18] to cover high-latitude areas of the Northern hemisphere
Summary
The SAR11 family Pelagibacteraceae [1] represents the most ubiquitous free-living lineage of heterotrophic bacteria in the world’s oceans [2, 3, 4, 5, 6, 7]. Successful cultivation efforts have paved the way for a functional understanding of SAR11 and elucidated their critical role in marine biogeochemical cycles [8, 9, 10, 11]. Their dominance in surface seawater has resulted in great interest to understand the diversity of SAR11 and their evolution in marine habitats [12]. A key study by Hellweger et al [16] simulated the evolution of a few cells for large numbers of generations under a neutral model, the results of which suggested that geographic patterns in marine microbial populations could emerge without selection due to slow-moving oceanic currents. The copyright holder for this preprint It is made available under of neutral evolution as the main source of intra-population genomic variation has not been empirically tested
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