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.
    Full-text · Article · Jun 2015 · Environmental Microbiology
    • "Some species of Ruegeria (e.g. Ruegeria pomeroyi) catabolize dimethylsulphoniopropionate (DMSP) produced by marine phytoplankton (Curson et al. 2011 ), and they therefore play an important role in the marine sulphur cycles. Although it remains to be seen whether these Ruegeria-like bacteria are autochthonous, the circumstantial evidence presented here implies that they could simply stem from ingested debris, which may or may not form part of their diet. "
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    ABSTRACT: Intestinal tracts are among the most densely populated microbial ecosystems. Gut microbiota and their influence on the host have been well characterized in terrestrial vertebrates but much less so in fish. This is especially true for coral reef fishes, which are among the most abundant groups of vertebrates on earth. Surgeonfishes (family: Acanthuridae) are part of a large and diverse family of reef fish that display a wide range of feeding behaviors, which in turn has a strong impact on the reef ecology. Here, we studied the composition of the gut microbiota of nine surgeonfish and three non-surgeonfish species from the Red Sea. High-throughput pyrosequencing results showed that members of the phylum Firmicutes, especially of the genus Epulopiscium, were dominant in the gut microbiota of seven surgeonfishes. Even so, there were large inter- and intra-species differences in the diversity of surgeonfish microbiota. Replicates of the same host species shared only a small number of operational taxonomic units (OTUs), although these accounted for most of the sequences. There was a statistically significant correlation between the phylogeny of the host and their gut microbiota, but the two were not completely congruent. Notably, the gut microbiota of three non-surgeonfish species clustered with some surgeonfish species. The microbiota of the macro- and micro-algavores were distinct, while the microbiota of the others (carnivores, omnivores and detritivores) seemed to be transient and dynamic. Despite some anomalies, both host phylogeny and diet were important drivers for the intestinal microbial community structure of surgeonfishes from the Red Sea. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    No preview · Article · Dec 2014 · Molecular Ecology
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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.
    Full-text · Article · Oct 2014 · The Journal of Microbiology
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