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  • Review Article
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Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes

Key Points

  • The anti-stress molecule dimethylsulphoniopropionate (DMSP) is made in vast quantities — about 1 billion tonnes per year — by many single-celled plankton and some algal seaweeds; when it is released by these organisms into the oceans, it is a food source for many marine bacteria. The importance of the associated catabolic biotransformations in the global sulphur cycle is all the more great because one of the products, the volatile dimethyl sulphide (DMS), has several environmental effects, ranging from the initiation of cloud cover by some of its oxidation products to its ability to act as a chemoattractant for many marine animals.

  • Recent genetic and genomic analyses of several marine bacteria have provided many insights into the mechanisms of DMSP catabolism. These insights include an unexpected amount of diversity in the enzymatic mechanisms and the regulation involved, and in the identities of the microorganisms that can degrade DMSP.

  • The dmd genes that encode enzymes of the demethylation pathway for DMSP catabolism occur in many strains of abundant marine alphaproteobacteria known as the roseobacters and also in the world's most populous group of marine bacteria, the SAR11 clade. These genes are therefore widespread in metagenomic data sets from marine environments. The demethylation pathway that was revealed by molecular genetics differed from that which had been previously predicted.

  • Another series of catabolic pathways involves the cleavage of DMSP by enzymes known generically as DMSP lyases, which generate dimethyl sulphide (DMS) as a primary product. A total of six enzymes, encoded by their corresponding ddd genes, were identified in different bacteria, and these differ with regard to their polypeptide families, their subcellular locations (one of them, DddY, is in the periplasm) and the identities of their catabolites. DddD generates 3-hydroxypropionate (3HP), whereas the other five — DddL, DddP, DddQ, DddW and DddY — give rise to acrylate.

  • Several ddd genes that encode different DMSP lyases are subject to horizontal gene transfer, in some cases between taxonomically diverse organisms. For example, DddP occurs not only in roseobacters, but also sporadically in other distantly related marine bacteria and, more remarkably, in some fungal pathogens.

  • Some individual bacteria have multiple ways of catabolizing DMSP. This feature is most prevalent in the roseobacters, several strains of which contain the DMSP demethylase and one or more different DMSP lyases. These different mechanisms may be adapted to particular environmental conditions.

  • In several bacteria, the regulation of DMSP cleavage is unusual, as the catabolic products, acrylate or 3HP, can act as co-inducers of the ddd genes and, hence, of the DMS-producing phenotype. Although the substrate DMSP may seem to be an effective co-inducer in some species, it must first be converted to one of the bona fide inducer molecules.

Abstract

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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Figure 1: The formation and catabolic fate of dimethylsulphoniopropionate.
Figure 2: Biochemical pathways for dimethylsulphoniopropionate degradation.
Figure 3: The ddd–acu gene clusters in Halomonas sp. HTNK1, Alcaligenes faecalis str. M3A and Marinomonas sp. MWYL1.

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Acknowledgements

The authors are grateful to M. Kirkwood, E. Fowler, C. Brearley, Y. Chan, L. Sun, S. Newton-Payne, N. Nikolaidou-Katsaridou and R. Green for helpful discussions. This work was funded by the UK Biotechnology and Biological Sciences Research Council and the UK National Environment Research Council.

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Zwitterion

A molecule that contains both a positive and a negative charge at different regions in the molecule.

Biotransformations

Conversions or modifications of starting compounds to form other compounds.

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The ability of an organism or cell to tolerate high concentrations of solutes.

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A compound, often a nutrient, towards which motile organisms (including bacteria, animals and protists) move.

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A polypeptide that affects the level of expression of a gene, usually by binding to cis-acting DNA sequences near the promoter of that gene.

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Curson, A., Todd, J., Sullivan, M. et al. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat Rev Microbiol 9, 849–859 (2011). https://doi.org/10.1038/nrmicro2653

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