Streamlining and Core Genome Conservation among Highly Divergent Members of the SAR11 Clade

Abstract

SAR11 is an ancient and diverse clade of heterotrophic bacteria that are abundant throughout the world’s oceans, where they play a major role in the ocean carbon cycle. Correlations between the phylogenetic branching order and spatiotemporal patterns in cell distributions from planktonic ocean environments indicate that SAR11 has evolved into perhaps a dozen or more specialized ecotypes that span evolutionary distances equivalent to a bacterial order. We isolated and sequenced genomes from diverse SAR11 cultures that represent three major lineages and encompass the full breadth of the clade. The new data expand observations about genome evolution and gene content that previously had been restricted to the SAR11 Ia subclade, providing a much broader perspective on the clade’s origins, evolution, and ecology. We found small genomes throughout the clade and a very high proportion of core genome genes (48 to 56%), indicating that small genome size is probably an ancestral characteristic. In their level of core genome conservation, the members of SAR11 are outliers, the most conserved free-living bacteria known. Shared features of the clade include low GC content, high gene synteny, a large hypervariable region bounded by rRNA genes, and low numbers of paralogs. Variation among the genomes included genes for phosphorus metabolism, glycolysis, and C1 metabolism, suggesting that adaptive specialization in nutrient resource utilization is important to niche partitioning and ecotype divergence within the clade. These data provide support for the conclusion that streamlining selection for efficient cell replication in the planktonic habitat has occurred throughout the evolution and diversification of this clade.

Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’

“…Many of the genomic streamlining features observed in Cand. IA genome, such as small genome size, small intergenic regions, low incidences of gene duplication and low number of rRNA operons, have been associated with specific trophic lifestyles, mainly oligotrophy and obligate symbiosis (Giovannoni et al, 2005;Lauro et al, 2009;Walker et al, 2010;Grote et al, 2012;Swan et al, 2013), where they appear to be a reflection of the accessibility of nutrients, as well as the occurrence of genetic drift in obligate symbionts (Mira et al, 2001;Wernegreen, 2002;Giovannoni et al, 2005;Oakeson et al, 2014). However, detailed comparative analysis of the metabolism and genomic features of Cand.…”

Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype

“…As would be expected from a low percentage of unique genes in the SAGs, much of the metabolism of these organisms appeared to be similar to that of the surface strains, particularly the subclade Ia organisms. Collectively, the Ic subclades were predicted to be obligate aerobic organisms, with cytochrome c oxidase as the sole predicted terminal reductatse, a complete tricarboxylic acid cycle, conserved lesions in several glycolytic pathways (Schwalbach et al, 2010), a reliance on reduced sulfur compounds (Tripp et al, 2008) and pathways for the metabolism and oxidation of small organic molecules such as amino/carboxylic acids and one-carbon and methylated compounds (Yilmaz et al, 2011;Grote et al, 2012;Carini et al, 2012;Supplementary Table S1).…”

“…Although the majority of research has focused on the SAR11 clade in the euphotic and upper mesopelagic zones, multiple studies have demonstrated evidence of substantial SAR11 populations deeper in the mesopelagic, as well as in the bathy-and even hadopelagic (46000 m) realms (Martin-Cuadrado et al, 2007;Konstantinidis et al, 2009;Schattenhofer et al, 2009;Quaiser et al, 2010;Swan et al, 2011;Eloe et al, 2011a, b;King et al, 2013). SAR11, or the 'Pelagibacterales,' is a diverse group, spanning at least 18% 16S rRNA gene divergence, and is comprised of subclades with unique spatiotemporal distributions (ecotypes) that follow seasonal patterns (Field et al, 1997;Carlson et al, 2009;Giovannoni and Vergin, 2012;Grote et al, 2012;Vergin et al, 2013). All genome-sequenced representatives are characterized by small (1.3-1.4 Mbp), streamlined genomes with low GC content, few gene duplications and an obligately aerobic, heterotrophic metabolism generally focused on oxidation of low-molecularweight carbon compounds, such as carboxylic and amino acids, osmolytes and methylated compounds (Schwalbach et al, 2010;Yilmaz et al, 2011;Carini et al, 2012;Grote et al, 2012).…”

“…All genome-sequenced representatives are characterized by small (1.3-1.4 Mbp), streamlined genomes with low GC content, few gene duplications and an obligately aerobic, heterotrophic metabolism generally focused on oxidation of low-molecularweight carbon compounds, such as carboxylic and amino acids, osmolytes and methylated compounds (Schwalbach et al, 2010;Yilmaz et al, 2011;Carini et al, 2012;Grote et al, 2012). Representatives spanning the known subclade diversity have an unusually high level of core genome conservation and gene synteny, however, some subclade-specific genomic features have been identified (Grote et al, 2012). The subclade V representative, HIMB59, encodes a complete glycolysis pathway and a variety of predicted sugar transporters.…”

“…SAR11, or the 'Pelagibacterales,' is a diverse group, spanning at least 18% 16S rRNA gene divergence, and is comprised of subclades with unique spatiotemporal distributions (ecotypes) that follow seasonal patterns (Field et al, 1997;Carlson et al, 2009;Giovannoni and Vergin, 2012;Grote et al, 2012;Vergin et al, 2013). All genome-sequenced representatives are characterized by small (1.3-1.4 Mbp), streamlined genomes with low GC content, few gene duplications and an obligately aerobic, heterotrophic metabolism generally focused on oxidation of low-molecularweight carbon compounds, such as carboxylic and amino acids, osmolytes and methylated compounds (Schwalbach et al, 2010;Yilmaz et al, 2011;Carini et al, 2012;Grote et al, 2012). Representatives spanning the known subclade diversity have an unusually high level of core genome conservation and gene synteny, however, some subclade-specific genomic features have been identified (Grote et al, 2012).…”