One Carbon Metabolism in SAR11 Pelagic Marine Bacteria

Abstract

The SAR11 Alphaproteobacteria are the most abundant heterotrophs in the oceans and are believed to play a major role in mineralizing marine dissolved organic carbon. Their genomes are among the smallest known for free-living heterotrophic cells, raising questions about how they successfully utilize complex organic matter with a limited metabolic repertoire. Here we show that conserved genes in SAR11 subgroup Ia (Candidatus Pelagibacter ubique) genomes encode pathways for the oxidation of a variety of one-carbon compounds and methyl functional groups from methylated compounds. These pathways were predicted to produce energy by tetrahydrofolate (THF)-mediated oxidation, but not to support the net assimilation of biomass from C1 compounds. Measurements of cellular ATP content and the oxidation of 14C-labeled compounds to 14CO2 indicated that methanol, formaldehyde, methylamine, and methyl groups from glycine betaine (GBT), trimethylamine (TMA), trimethylamine N-oxide (TMAO), and dimethylsulfoniopropionate (DMSP) were oxidized by axenic cultures of the SAR11 strain Ca. P. ubique HTCC1062. Analyses of metagenomic data showed that genes for C1 metabolism occur at a high frequency in natural SAR11 populations. In short term incubations, natural communities of Sargasso Sea microbial plankton expressed a potential for the oxidation of 14C-labeled formate, formaldehyde, methanol and TMAO that was similar to cultured SAR11 cells and, like cultured SAR11 cells, incorporated a much larger percentage of pyruvate and glucose (27–35%) than of C1 compounds (2–6%) into biomass. Collectively, these genomic, cellular and environmental data show a surprising capacity for demethylation and C1 oxidation in SAR11 cultures and in natural microbial communities dominated by SAR11, and support the conclusion that C1 oxidation might be a significant conduit by which dissolved organic carbon is recycled to CO2 in the upper ocean.

Implications of streamlining theory for microbial ecology

“…One of the surprises of Pelagibacter metabolism was the discovery that they devote part of their genome to one-carbon (C1) metabolism. C1 metabolism enables Pelagibacterales to oxidize a broad range of external metabolites, including C1 compounds, such as methanol and formaldehyde, and methylated compounds, including osmolytes (glycine betaine, taurine, 3-dimethyl-sulfoniopropionate and trimethylamine oxide; Sun et al, 2011). Osmolytes, also known as compatible solutes, are fundamental compounds in the sense that they are produced in large amounts by all cells in marine systems.…”

Climate relevant trace gases (N2O and CH4) in the Eurasian Basin (Arctic Ocean)

“…Interestingly, several surface stations (ST 4, 5, 8 and 1) displayed CH 4 saturation levels as high as 650%. Although it remains unclear at present how CH 4 is formed in sea ice, it is possible that CH 4 could be produced via the methylotrophic pathway mediated by methylated compounds (Schäfer, 2007;Sun et al, 2011). One candidate for methylated compounds is DMSP and/or DMS, as indicated in the surface water by Damm et al (2010) and Florez-Leiva et al (2013).…”

Methane production induced by dimethylsulfide in surface water of an upwelling ecosystem

“…P. ubique HTCC1062; Sun et al, 2011) indicate that these microorganisms, some of the most abundant heterotrophic bacteria in surface waters, have genes that encode for oxidation pathways of a variety of one-carbon compounds, and they possess the capacity for demethylation and C1 oxidation, but do not incorporate C1 as biomass. These findings suggest the important role of this assemblage in obtaining energy from these compounds, and in mediating dissolved organic carbon cycling into CO 2 in the upper ocean (Sun et al, 2011).…”

“…P. ubique HTCC1062; Sun et al, 2011) indicate that these microorganisms, some of the most abundant heterotrophic bacteria in surface waters, have genes that encode for oxidation pathways of a variety of one-carbon compounds, and they possess the capacity for demethylation and C1 oxidation, but do not incorporate C1 as biomass. These findings suggest the important role of this assemblage in obtaining energy from these compounds, and in mediating dissolved organic carbon cycling into CO 2 in the upper ocean (Sun et al, 2011). Neufeld et al (2008) demonstrated that active marine methylotrophs belonging to the Alphaproteobacteria and Gammaproteobacteria are associated with phytoplankton blooms in coastal environments, which in turn, and depending on the phytoplankton species, provide substrates for methylotrophs and mediate CH 4 production.…”