Catabolism of dimethylsulphoniopropionate: Microorganisms

School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK.
Nature Reviews Microbiology (Impact Factor: 23.57). 12/2011; 9(12):849-59. DOI: 10.1038/nrmicro2653
Source: PubMed


The compatible solute dimethylsulphoniopropionate (DMSP) has important roles in marine environments. It is an anti-stress compound made by many single-celled plankton, some seaweeds and a few land plants that live by the shore. Furthermore, in the oceans it is a major source of carbon and sulphur for marine bacteria that break it down to products such as dimethyl sulphide, which are important in their own right and have wide-ranging effects, from altering animal behaviour to seeding cloud formation. In this Review, we describe how recent genetic and genomic work on the ways in which several different bacteria, and some fungi, catabolize DMSP has provided new and surprising insights into the mechanisms, regulation and possible evolution of DMSP catabolism in microorganisms.

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    • "BetA belongs to the glucose-methanol-choline (GMC) oxidoreductase family (Cavener, 1992), including the characterized 3-hydroxypropionate dehydrogenase (DddA) which is involved in DMSP catabolism (Curson et al., 2011). In addition to the MRC clade, BetA is also found in many isolates from the Gammaproteobacteria, including Vibrio spp. "
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    ABSTRACT: Choline is ubiquitous in marine eukaryotes and appears to be widely distributed in surface marine waters; however its metabolism by marine bacteria is poorly understood. Here, using comparative genomics and molecular genetic approaches, we reveal that the capacity for choline catabolism is widespread in marine heterotrophs of the marine Roseobacter clade (MRC). Using the model bacterium Ruegeria pomeroyi, we confirm that the betA, betB and betC genes, encoding choline dehydrogenase, betaine aldehyde dehydrogenase and choline sulfatase, respectively, are involved in choline metabolism. The betT gene, encoding an organic solute transporter, was essential for the rapid uptake of choline but not glycine betaine (GBT). Growth of choline and GBT as a sole carbon source resulted in the re-mineralisation of these nitrogen-rich compounds into ammonium. Oxidation of the methyl groups from choline requires formyltetrahydrofolate synthetase encoded by fhs in R. pomeroyi, deletion of which resulted in incomplete degradation of GBT. We demonstrate that this was due to an imbalance in the supply of reducing equivalents required for choline catabolism, which can be alleviated by the addition of formate. Together, our results demonstrate that choline metabolism is ubiquitous in MRC and reveal the role of Fhs in methyl group oxidation in R. pomeroyi. This article is protected by copyright. All rights reserved.
    Environmental Microbiology 06/2015; DOI:10.1111/1462-2920.12943 · 6.20 Impact Factor
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    • "Once released into the extracellular environment by viral lysis, algal senescence, zooplankton grazing on phytoplankton, or physiological stress (Hill et al., 1998; Laroche et al., 1999; Kiene et al., 2000; Mulholland and Otte, 2002) the dissolved DMSP (DMSPd) can be rapidly catabolized via two pathways which are microbially mediated: cleavage and demethylation/demethiolation (Visscher et al., 1992; Yoch, 2002). Although the cleavage pathway represents a considerable source of DMS (Curson et al., 2011), demethylation/demethiolation produces the highly reactive volatile sulfur compound methanethiol (MeSH). "
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    ABSTRACT: Dimethylsulfoniopropionate (DMSP) is an important carbon and sulfur source to marine bacterial communities and the main precursor of dimethylsulfide (DMS), a gas that influences atmospheric chemistry and potentially the global climate. In nature, bacterial DMSP catabolism can yield different proportions of DMS and methanethiol (MeSH), but relatively little is known about the factors controlling the pathways of bacterial degradation that select between their formation (cleavage vs. demethiolation). In this study, we carried out experiments to evaluate the influence of salinity on the routes of DMSP catabolism in Ruegeria pomeroyi DSS-3. We monitored DMS and MeSH accumulation in cell suspensions grown in a range of salinities (10, 20, 30 ppt) and with different DMSP amendments (0, 50, 500 μM). Significantly higher concentrations of DMS accumulated in low salinity treatments (10 ppt; P < 0.001), in both Marine Basal Medium (MBM) and half-strength Yeast Tryptone Sea Salts (1/2 YTSS) media. Results showed a 47.1% and 87.5% decrease of DMS accumulation, from salinity 10 to 20 ppt, in MBM and 1/2YTSS media, respectively. On the other hand, MeSH showed enhanced accumulations at higher salinities (20, 30 ppt), with a 90.6% increase of MeSH accumulation from the 20 ppt to the 30 ppt salinity treatments. Our results with R. pomeroyi DSS-3 in culture are in agreement with previous results from estuarine sediments and demonstrate that salinity can modulate selection of the DMSP enzymatic degradation routes, with a consequent potential impact on DMS and MeSH liberation into the atmosphere.
    The Journal of Microbiology 10/2014; 52(11). DOI:10.1007/s12275-014-4409-1 · 1.44 Impact Factor
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    • "(Adapted from [1]). A complete depiction of catabolic processing of DMSP by microbes is detailed in [6]. "
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    ABSTRACT: Marine microbes degrade dimethylsulfoniopropionate (DMSP), which is produced in large quantities by marine algae and plants, with DMSP lyases into acrylate and the gas dimethyl sulfide (DMS). Approximately 10% of the DMS vents from the sea into the atmosphere and this emission returns sulfur, which arrives in the sea through rivers and runoff, back to terrestrial systems via clouds and rain. Despite their key role in this sulfur cycle DMSP lyases are poorly understood at the molecular level. Here we report the first X-ray crystal structure of the putative DMSP lyase RdDddP from Roseobacter denitrificans, which belongs to the abundant DddP family. This structure, determined to 2.15 Å resolution, shows that RdDddP is a homodimeric metalloprotein with a binuclear center of two metal ions located 2.7 Å apart in the active site of the enzyme. Consistent with the crystallographic data, inductively coupled plasma mass spectrometry (ICP-MS) and total reflection X-ray fluorescence (TRXF) revealed the bound metal species to be primarily iron. A 3D structure guided analysis of environmental DddP lyase sequences elucidated the critical residues for metal binding are invariant, suggesting all proteins in the DddP family are metalloenzymes.
    PLoS ONE 07/2014; 9(7):e103128. DOI:10.1371/journal.pone.0103128 · 3.23 Impact Factor
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