Catabolism of dimethylsulphoniopropionate: Microorganisms, enzymes and genes

ArticleinNature Reviews Microbiology 9(12):849-59 · December 2011with50 Reads
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.
    • "This method had been used during a previous mesocosm experiment (SOPRAN II, Bergen, Norway), and the results correlated well with those measured immediately on a similar GC-FPD system (Webb et al., 2015). It was considered unlikely that rates of bacterial DMSP turnover through demethylation rather than through cleavage to produce DMS (Curson et al., 2011) were sufficiently high in the Baltic Sea to remove all detectable DMSP yet still produce measurable DMS concentrations. Also, rapid turnover of dissolved DMSP in surface waters being the cause of low DMSP T concentrations does not explain the lack of intracellular particulate-phase DMSP. "
    [Show abstract] [Hide abstract] ABSTRACT: The Baltic Sea is a unique environment as the largest body of brackish water in the world. Acidification of the surface oceans due to absorption of anthropogenic CO2 emissions is an additional stressor facing the pelagic community of the already challenging Baltic Sea. To investigate its impact on trace gas biogeochemistry, a largescale mesocosm experiment was performed off Tvärminne Research Station, Finland, in summer 2012. During the second half of the experiment, dimethylsulfide (DMS) concentrations in the highest-fCO2 mesocosms (1075-1333 μatm) were 34% lower than at ambient CO2 (350 μatm). However, the net production (as measured by concentration change) of seven halocarbons analysed was not significantly affected by even the highest CO2 levels after 5 weeks' exposure. Methyl iodide (CH3I) and diiodomethane (CH2I2) showed 15 and 57% increases in mean mesocosm concentration (3.8±0.6 increasing to 4.3±0.4 pmol L⁻¹ and 87.4±14.9 increasing to 134.4±24.1 pmol L⁻¹ respectively) during Phase II of the experiment, which were unrelated to CO2 and corresponded to 30% lower Chl a concentrations compared to Phase I. No other iodocarbons increased or showed a peak, with mean chloroiodomethane (CH2ClI) concentrations measured at 5.3 (±0.9) pmol L⁻¹ and iodoethane (C2H5I) at 0.5 (±0.1) pmol L⁻¹. Of the concentrations of bromoform (CHBr3; mean 88.1±13.2 pmol L⁻¹), dibromomethane (CH2Br2; mean 5.3±0.8 pmol L⁻¹), and dibromochloromethane (CHBr2Cl, mean 3.0±0.5 pmol L⁻¹), only CH2Br2 showed a decrease of 17% between Phases I and II, with CHBr3 and CHBr2Cl showing similar mean concentrations in both phases. Outside the mesocosms, an upwelling event was responsible for bringing colder, high-CO2, low-pH water to the surface starting on day t16 of the experiment; this variable CO2 system with frequent upwelling events implies that the community of the Baltic Sea is acclimated to regular significant declines in pH caused by up to 800 μatm fCO2. After this upwelling, DMS concentrations declined, but halocarbon concentrations remained similar or increased compared to measurements prior to the change in conditions. Based on our findings, with future acidification of Baltic Sea waters, biogenic halocarbon emissions are likely to remain at similar values to today; however, emissions of biogenic sulfur could significantly decrease in this region.
    Full-text · Article · Aug 2016
    • "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. "
    [Show abstract] [Hide abstract] 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
    • "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. "
    [Show abstract] [Hide abstract] 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.
    Article · Dec 2014
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