The Evolutionary Success of the Marine Bacterium SAR11 Analyzed through a Metagenomic Perspective

Abstract

The SAR11 clade of Alphaproteobacteria is the most abundant group of planktonic cells in the near-surface epipelagic waters of the ocean, but the mechanisms underlying its exceptional success have not been fully elucidated. Here, we applied a metagenomic approach to explore microdiversity patterns by measuring the accumulation of synonymous and nonsynonymous mutations as well as homologous recombination in populations of SAR11 from different aquatic habitats (marine epipelagic, bathypelagic, and surface freshwater). The patterns of mutation accumulation and recombination were compared to those of other groups of representative marine microbes with multiple ecological strategies that share the same marine habitat, namely, Cyanobacteria (Prochlorococcus and Synechococcus), Archaea (“Candidatus Nitrosopelagicus” and Marine Group II Thalassoarchaea), and some heterotrophic marine bacteria (Alteromonas and Erythrobacter). SAR11 populations showed widespread recombination among distantly related members, preventing divergence leading to a genetically stable population. Moreover, their high intrapopulation sequence diversity with an enrichment in synonymous replacements supports the idea of a very ancient divergence and the coexistence of multiple different clones. However, other microbes analyzed seem to follow different evolutionary dynamics where processes of diversification driven by geographic and ecological instability produce a higher number of nonsynonymous replacements and lower intrapopulation sequence diversity. Together, these data shed light on some of the evolutionary and ecological processes that lead to the large genomic diversity in SAR11. Furthermore, this approach can be applied to other similar microbes that are difficult to culture in the laboratory, but abundant in nature, to investigate the underlying dynamics of their genomic evolution. IMPORTANCE As the most abundant bacteria in oceans, the Pelagibacterales order (here SAR11) plays an important role in the global carbon cycle, but the study of the evolutionary forces driving its evolution has lagged considerably due to the inherent difficulty of obtaining pure cultures. Multiple evolutionary models have been proposed to explain the diversification of distinct lineages within a population; however, the identification of many of these patterns in natural populations remains mostly enigmatic. We have used a metagenomic approach to explore microdiversity patterns in their natural habitats. Comparison with a collection of bacterial and archaeal groups from the same environments shows that SAR11 populations have a different evolutionary regime, where multiple genotypes coexist within the same population and remain stable over time. Widespread homologous recombination could be one of the main driving factors of this homogenization.

Genomes of the “ Candidatus Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria

“…Actinomarinales” species that are made up of discrete populations with an ANIr of ca. 97%, similar to other nonstreamlined genomes ( 27 ), suggesting fewer concurrent species or less interspecies recombination. Another major difference at the level of comparative population genomics between these two streamlined microbes is the size of the core genome, ca.…”

“…4B ). In contrast, Pelagibacterales populations are characterized by ANIr values below 95%, and the threshold in the linear recruitment plots is located above 80% identity, suggesting much higher intrapopulation diversity ( 27 ).…”

“…One recent discovery about at least some Pelagibacterales species is that they are present in nature in populations with low ANIr (ca. 92%), i.e., they have high intrapopulation diversity that among other reasons could be attributed to very high levels of recombination (intra- and interspecies) ( 27 ). This does not seem to hold for “ Ca.…”

Phylogenomics of SAR116 clade reveals two subclades with different evolutionary trajectories and important role in the ocean sulfur cycle

“…We found that the median dN/dS value was ca. 0.09 for LGC, this value was comparable to the better known marine SAR11 clade (34) and suggests a strong purifying selection acting on the genome evolution of this subclade (Table S3). Within the HGC subclass, we observed much more variable values.…”

“…These genomic features suggested that members within the LGC subclade are undergoing a streamlining process without genome reduction. For that reason, we studied other characteristic genomic parameters that have been proposed to be relevant in the streamlined genomes such as selective pressure and the number of paralogs (34)(35)(36)(37). Microevolution was measured as the ratio of nonsynonymous to synonymous polymorphisms (dN/dS ratio).…”