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.
Highlights
C1 metabolism takes place through a network of interrelated biochemical reactions that involves the transfer of one-carbon units from one compound to another
To evaluate the conservation and diversity of C1 oxidation pathways in SAR11 we examined the distribution of genes for C1 metabolism among three SAR11 genomes of the Group Ia subclade, and these genes were found in all three SAR11 Ia genomes (Table 1)
We found the homolog of gamma-glutamylmethylamide synthetase (GMAS) from this pathway in HTCC1062, which was annotated as glnT, a glutamine synthetase III (SAR11_1316, Fig. 1C) and shares the conserved Gln-synt_C domain (Pfam PF00120.17) with GMAS
Summary
C1 metabolism takes place through a network of interrelated biochemical reactions that involves the transfer of one-carbon units from one compound to another. A few specialized bacteria oxidize methyl groups and C1 compounds, such as methanol, formaldehyde, formate and methylamine, to derive energy and cellular carbon. Marine dissolved organic carbon (DOC) includes a diverse array of C1 and methylated compounds that are potential substrates for C1 oxidation. Sources of seawater formaldehyde are atmospheric deposition from industrial emissions and the photo-oxidation of atmospheric hydrocarbons [15,16], and the photo-oxidation of dissolved organic carbon in the ocean surface [17]. Formaldehyde is a key reactive intermediate in bacterial metabolism of C1 growth substrates like methane or methanol [19,20,21], and it is a central intermediate of GBT methyl group oxidation [22]. Due to its nonspecific reactivity with proteins and DNA, formaldehyde is toxic to cells, and many studies have examined mechanisms by which organisms can remove this potentially lethal compound [23,24]
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