Metabolism of dimethylsulphoniopropionate by Ruegeria pomeroyi DSS‐3

Abstract

SummaryRuegeria pomeroyi DSS-3 possesses two general pathways for metabolism of dimethylsulphoniopropionate (DMSP), an osmolyte of algae and abundant carbon source for marine bacteria. In the DMSP cleavage pathway, acrylate is transformed into acryloyl-CoA by propionate-CoA ligase (SPO2934) and other unidentified acyl-CoA ligases. Acryloyl-CoA is then reduced to propionyl-CoA by AcuI or SPO1914. Acryloyl-CoA is also rapidly hydrated to 3-hydroxypropionyl-CoA by acryloyl-CoA hydratase (SPO0147). A SPO1914 mutant was unable to grow on acrylate as the sole carbon source, supporting its role in this pathway. Similarly, growth on methylmercaptopropionate, the first intermediate of the DMSP demethylation pathway, was severely inhibited by a mutation in the gene encoding crotonyl-CoA carboxylase/ reductase, demonstrating that acetate produced by this pathway was metabolized by the ethylmalonylCoA pathway. Amino acids and nucleosides from cells grown on 13 C-enriched DMSP possessed labelling patterns that were consistent with carbon from DMSP being metabolized by both the ethylmalonyl-CoA and acrylate pathways as well as a role for pyruvate dehydrogenase. This latter conclusion was supported by the phenotype of a pdh mutant, which grew poorly on electron-rich substrates. Additionally, label from [ 13 Cmethyl] DMSP only appeared in carbons derived from methyl-tetrahydrofolate, and there was no evidence for a serine cycle of C-1 assimilation.

The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol

“…The DMSP lyases dddK and dddQ, and dddP, the putative lyase with low activity, were 2 much less abundant than dmdABC or the single-copy marker recA. This supports the 3 interpretation that either the cleavage pathway is less important than the demethylation pathway, 4 or undiscovered DMSP lyase analogs are present in other Pelagibacterales strains. Interestingly, 5 Pelagibacterales genes for metabolism of acrylate are more abundant than DMSP lyases, and 6 similar in abundance to demethylation genes and recA, which supports either the interpretation 7 that DMSP lyases are underestimated because of their diversity, or that Pelagibacter cells 8 lacking DMSP lyase use acrylate from other sources, perhaps dissolved acrylate.…”

“…2 The model presented in Fig. S8 captures the observations we report, and provides an 3 explanation for why cells might simultaneously express two pathways that compete for a single 4 substrate. Although the model in Fig.…”

“…2A). 1 We propose that constitutive, simultaneous expression of the cleavage and demethylation 2 pathways in Pelagibacter is an adaptation that provides these cells with a kinetically regulated 3 system that favors the pathway to DMS formation when intracellular DMSP concentrations are 4 high. We modeled this process (Fig.…”

“…Also reported in nearly all 1 Pelagibacterales are genes encoding methyl group oxidation pathways (Fig. S1), which 2 produce energy from DMSP demethylation and are essential to the demethylation pathway 3 because they perform the function of regenerating the methyl-group-accepting cofactor 4 tetrahydrofolate (THF) 15,20 . Pelagibacterales strains also contain homologs of cystathionine-5 gamma-synthetase (cys-γ-synth), predicted to catalyze the conversion of MeSH to methionine 21 , 6 and thus necessary for growth using MeSH as a sole sulfur source.…”

“…3). To test the capacity 4 of strain HTCC1062 to assimilate acrylate, propionate or 3-HP, we relied on the unusual 5 requirement of Pelagibacter strains for growth substrates that can be metabolized to pyruvate, 6 which these cells require for alanine synthesis 16 . As predicted, acrylate and propionate each 7 could substitute for pyruvate in defined media.…”