Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria

Abstract

Dimethylsulphoniopropionate (DMSP) accounts for up to 10% of carbon fixed by marine phytoplankton in ocean surface waters, producing an estimated 11.7-103 Tmol S per year, most of which is processed by marine bacteria through the demethylation/demethiolation pathway. This pathway releases methanethiol (MeSH) instead of the climatically active gas dimethylsulphide (DMS) and enables marine microorganisms to assimilate the reduced sulphur. Despite recognition of this critical microbial transformation for over two decades, the biochemical pathway and enzymes responsible have remained unidentified. Here we show that three new enzymes related to fatty acid β-oxidation constitute the pathway that assimilates methylmercaptopropionate (MMPA), the first product of DMSP demethylation/demethiolation, and that two previously unknown coenzyme A (CoA) derivatives, 3-methylmercaptopropionyl-CoA (MMPA-CoA) and methylthioacryloyl-CoA (MTA-CoA), are formed as novel intermediates. A member of the marine roseobacters, Ruegeria pomeroyi DSS-3, requires the MMPA-CoA pathway for MMPA assimilation and MeSH production. This pathway and the ability to produce MeSH from MMPA are present in diverse bacteria, and the ubiquitous SAR11 clade bacterium Pelagibacter ubique possesses enzymes for at least the first two steps. Analysis of marine metagenomic data indicates that the pathway is widespread among bacterioplankton in the ocean surface waters, making it one of the most important known routes for acquisition of reduced carbon and sulphur by surface ocean heterotrophs.

Single-taxon field measurements of bacterial gene regulation controlling DMSP fate

“…Demethylation pathway gene dmdB (methylymercaptopropionate CoA-ligase; Reisch et al, 2011) and cleavage pathway genes prpE and acuI (propionyl-CoA synthetase and acrylate utilization protein; Todd et al, 2012) were present in abundances equal to dmdA and dddP (Supplementary Figure S4), consistent with expectations for single-copy genes in the same genomes. The transcription of these genes during the October 4-14 decoupled expression period for dmdA and dddP was correlated within a pathway but not between competing pathways.…”

“…This 'bacterial sulfur demand' hypothesis proposes that demethylation is favored by marine bacteria when reduced sulfur is limiting because the sulfur from DMSP can be assimilated into biomass through the demethylation pathway but not the cleavage pathway (Todd et al, 2009). However, sulfur may also be available to bacteria from organic compounds other than DMSP (Weinitschke et al, 2006;Reisch et al, 2011;Durham et al, 2014). Thus, the hypothesis proposes that when DMSP is the predominant source of available organic sulfur (relative to other organic sulfur compounds, not based on absolute Figure 2 Modified version of the bacterial sulfur demand conceptual model applied to Monterey Bay, CA, USA populations of Roseobacter HTCC2255 showing differential regulation of DMSP demethylation and cleavage pathways.…”

“…Laboratory qPCR assays of DMSP genes and transcripts used similar conditions and primer/probe concentrations as for the ESP (Supplementary Table S1). Primers were designed for five additional HTCC2255 genes: downstream demethylation pathway gene dmdB (methylymercaptopropionate CoAligase; Reisch et al, 2011), downstream cleavage pathway genes prpE and acuI (propionyl-CoA synthetase and acrylate utilization protein; Todd et al, 2012), and reactive oxygen species genes sodD (superoxide dismutase) and katG (catalase) (Supplementary Table S1), and qPCR was carried out for all genes on an iCycler iQ or iCycler iQ5 (BioRad, Hercules, CA, USA). For reverse-transcription (RT)-qPCR, the Invitrogen OneStep Express kit (SuperScript III) or SYBR One-step supermix for specific priming of cDNA synthesis was used in 25 ml final volumes.…”

Structures of dimethylsulfoniopropionate‐dependent demethylase from the marine organism Pelagabacter ubique

“…Interestingly, we observed two monomers in the asymmetric unit for DmdA with some domain swapping at the N-terminus for residues 1-11. These observations are consistent with previous work that has shown DmdA functions as a dimer in solution 5,6 (see Fig. 2, Panel A).…”

“…3,4 While some phytoplankton can convert DMSP to dimethyl sulfide (DMS), upon phytoplankton lysis a considerable amount of DMSP is released and rapidly metabolized by the marine microbial food web. 5 Marine bacterioplankton are considered to be the primary mediators of DMSP conversion in seawater and the consumption of DMSP by these organisms accounts for 1-15% of their carbon demand and most of their demand for sulfur. [6][7][8] The degradation of DMSP by marine bacteria occurs through two competing pathways, with either cleavage or demethylation as the first step.…”