Abstract
ABSTRACTThe SAR116 clade within the class Alphaproteobacteria represents one of the most abundant groups of heterotrophic bacteria inhabiting the surface of the ocean. The small number of cultured representatives of SAR116 (only two to date) is a major bottleneck that has prevented an in-depth study at the genomic level to understand the relationship between genome diversity and its role in the marine environment. In this study, we use all publicly available genomes to provide a genomic overview of the phylogeny, metabolism, and biogeography within the SAR116 clade. This increased genomic diversity has led to the discovery of two subclades that, despite coexisting in the same environment, display different properties in their genomic makeup. One represents a novel subclade for which no pure cultures have been isolated and is composed mainly of single-amplified genomes (SAGs). Genomes within this subclade showed convergent evolutionary trajectories with more streamlined features, such as low GC content (ca. 30%), short intergenic spacers (<22 bp), and strong purifying selection (low ratio of nonsynonymous to synonymous polymorphisms [dN/dS]). Besides, they were more abundant in metagenomic databases recruiting at the deep chlorophyll maximum. Less abundant and restricted to the upper photic layers of the global ocean, the other subclade of SAR116, enriched in metagenome-assembled genomes (MAGs), included the only two pure cultures. Genomic analysis suggested that both clades have a significant role in the sulfur cycle with differences in the way both clades can metabolize dimethylsulfoniopropionate (DMSP).IMPORTANCE The SAR116 clade of Alphaproteobacteria is a ubiquitous group of heterotrophic bacteria inhabiting the surface of the ocean, but the information about their ecology and population genomic diversity is scarce due to the difficulty of getting pure culture isolates. The combination of single-cell genomics and metagenomics has become an alternative approach to study these kinds of microbes. Our results expand the understanding of the genomic diversity, distribution, and lifestyles within this clade and provide evidence of different evolutionary trajectories in the genomic makeup of the two subclades that could serve to illustrate how evolutionary pressure can drive different adaptations to the same environment. Therefore, the SAR116 clade represents an ideal model organism for the study of the evolutionary streamlining of genomes in microbes that have relatively close relatedness to each other.
Highlights
IMPORTANCE The SAR116 clade of Alphaproteobacteria is a ubiquitous group of heterotrophic bacteria inhabiting the surface of the ocean, but the information about their ecology and population genomic diversity is scarce due to the difficulty of getting pure culture isolates
A total of 185 genomes were downloaded from publicly available databases putatively classified as members of the SAR116 clade, which includes only two cultured representatives (IMCC1322 and HIMB100) together with 120 singleamplified genomes (SAGs) and 63 metagenome-assembled genomes (MAGs) that met the established quality criteria of $50% completeness and #5% contamination, i.e., medium- to high-quality draft genomes [41]
The two pure culture representatives were placed in the same family (Puniceispirillaceae) that together with family UBA1172 clustered within one of the subclades characterized by containing a higher proportion of MAGs (59 MAGs and 43 SAGs) (Fig. 1A and B and Fig. S1)
Summary
IMPORTANCE The SAR116 clade of Alphaproteobacteria is a ubiquitous group of heterotrophic bacteria inhabiting the surface of the ocean, but the information about their ecology and population genomic diversity is scarce due to the difficulty of getting pure culture isolates. Molecular approaches targeting the 16S rRNA gene, such as fluorescence in situ hybridization (FISH), terminal restriction fragment length polymorphism (T-RFLP), and denaturing gradient gel electrophoresis (DGGE) and later the advent of next-generation DNA sequencing technologies, i.e., metagenomics, have proven that the surface ocean microbiome is mostly dominated by oligotrophs [15,16,17,18,19] Despite their abundance and importance, the bottleneck of acquiring pure cultures by classical culture-based approaches has considerably impeded their study. This minimization of cell size and complexity is coupled with highly compacted genomes characterized by (i) significant reduction in genome size with highly conserved core genomes and few pseudogenes, (ii) short intergenic spacers, (iii) low numbers of paralogs, and (iv) low GC content These genomic features described as an evolutionary adaptation for more efficient use of nutrients in oligotrophic environments removing nonessential genes are referred to as “streamlining theory” [25]. Despite playing a central role in the function of marine ecosystems, they have received much less attention largely because only a few isolates have been isolated or characterized [29], and most of our knowledge about their ecological and genomic role comes from either metagenome-assembled genomes (MAGs) or single-cell genomes (SAGs)
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