Single-amino acid variants reveal evolutionary processes that shape the biogeography of a global SAR11 subclade

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.

Accurate and Complete Genomes from Metagenomes

“…However, a genome reconstructed from a clonal microbial culture also does not represent the cloud of biologically important variation that exists in the natural population from where the isolate was derived. Population diversity can be analyzed by comparing all individual sequences (or short reads) to the metagenome-assembled reference genome (Simmons et al 2008;Delmont et al 2019) . While some populations are near-clonal, others are very complex strain mixtures and yet others fall on the continuum between these (Lo et al 2007;Chivian et al 2008;Simmons et al 2008) .…”

Accurate and complete genomes from metagenomes

“…However, a genome reconstructed from a clonal microbial culture also does not represent the cloud of biologically important variation that exists in the natural population from where the isolate was derived. Population diversity can be analyzed by comparing all individual sequences (or short reads) to the metagenome-assembled reference genome (Simmons et al 2008;Delmont et al 2019). Although some populations are near-clonal, others are very complex strain mixtures, and yet others fall on the continuum between these (Lo et al 2007; Chivian et al 2008;Simmons et al 2008).…”

Revealing ecologically coherent population structure of uncultivated bacterioplankton with POGENOM

“…Schloissnig et al 23 conducted pioneering cross-continental comparative analyses of human gut microbiomes using this approach and showed that there is more intraspecific genetic differentiation between habitats (human individuals) than within the same habitat over time. Similar approaches have been used by Nayfach et al 10 and Delmont et al 24 to show that gene content and amino acid composition, respectively, differ between oceanic regions within individual bacterial species.…”

“…Our results suggest that bacterioplankton do not only modulate the flexible gene pool when confronted by environmental clines, as demonstrated by several studies 10,52,53 , but also adapt by modifying existing genes (altering allele frequencies) to the different environmental conditions. Delmont 24 suggested an evolutionary mechanism for such conservation of genetic heterogeneity by emphasizing the role of consistent purifying selection against deleterious non-synonymous variants, exemplified by the cosmopolitan SAR11 clade. The same authors showed a partitioning of SAR11 metagenomes in concordance with large-scale oceanic temperatures suggesting that environmental selection is of central importance even at the microdiversity level in marine bacterioplankton.…”