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Microbial cycling of volatile organic sulfur compounds

RESEARCH LEADER: Dr Hendrik Schäfer

Dimethylsulfide is a key intermediate in the global sulfur cycle

Dimethylsulfide (DMS) is an organic sulfur gas that is emitted in large quantities from the marine environment and which accounts for the majority of biogenic atmospheric sulfur inputs. Its atmospheric oxidation products backscatter heat radiation and promote cloud formation, giving DMS a role in affecting atmospheric chemistry and climate (Charlson et al. 1987). Emission of DMS to the atmosphere also provides for a route of sulfur transport from the marine environment to the terrestrial environment via the atmosphere.

DMS degradation by microorganisms in the oceans has a major effect on the amount of sulfur that is available for sea-to-air transfer (Kiene & Bates, 1990). In soils, microbial degradation of DMS and other methylated sulfur compounds regenerates organically bound sulfur into the inorganic pool, a process that contributes to maintaining soil fertility. Microorganisms degrading DMS in terrestrial and marine environments therefore have an important role in affecting sulfur fluxes in the biosphere (reviewed in Schäfer et al. 2010).

Biochemistry, genetics and ecology of dimethylsulfide-degrading bacteria

Metabolism of DMS in bacteria is poorly understood at the molecular level which makes it challenging to assess which organisms and metabolic pathways are responsible for cycling of DMS and related organic sulfur compounds such as methanethiol (MT), dimethylsulfoxide (DMSO) in the environment. Our aim is to characterise enzymes and genes responsible for DMS degradation in order to gain a better understanding of global cycling of organic sulfur compounds.

An example is the classical key enzyme DMS monooxygenase which we identified in Hyphomicrobium sulfonivorans (Boden et al. 2011a). The idenfication of this previously uncharacterised enzyme now facilitates comparative genomics and proteomics work of DMS degrading bacteria, which play important roles in the environment and industrial processes, by degrading odorous DMS (eg in waste water treatment and biofiltration).

A major fate of DMS in the oceans is its degradation to DMSO. Our work has shown that in some bacteria such as Sagittula stellata, a marine bacterial isolate that does not grow on DMS, the oxidation of DMS to DMSO can be used as a source of energy (Boden et al. 2011b).

Perhaps a more significant pathway of DMS to DMSO oxidation is the discovery of a co-oxidation pathway in marine bacteria. In Ruegeria pomeroyi, a representative of the abundant marine Roseobacter clade (Lidbury et al. 2016) that does not grow on DMS, but which can utilise methylated amines as N-source, the enzyme trimethylamine monooxygenase co-oxidises DMS to DMSO.

Ecology of DMS-degrading microorganims

Using molecular biological approaches, stable isotope probing and metagenomics, we are making progress in identifying methylotrophic microorganisms (organisms able to grow on one-carbon compounds) that contribute to DMS cycling in the marine and terrestrial environment. Our work using stable isotope probing shows that in the marine environment, gammaproteobacteria related to the genus Methylophaga are able to assimilate DMS carbon (Schäfer 2007; Neufeld et al. 2008), whereas uncultivated populations related to Methylophilaceae and Thiobacillus spp. contribute to DMS degradation in soil and lake sediments (Eyice et al. 2015).


LITERATURE

Boden, R., Borodina, E., Wood, A.P., Kelly, D.P., Murrell, J.C., and H. Schäfer (2011a). Purification and characterization of dimethylsulfide monooxygenase from Hyphomicrobium sulfonivorans. J. Bact. 193, 1250-1258. DOI: 10.1128/JB.00977-10.

Boden, R., Murrell, J.C., and H. Schäfer (2011b). Dimethylsulfide is an energy source for the heterotrophic marine bacterium Sagittula stellata. FEMS Microbiol Lett. 322, 188-193.

Boden, R., Ferriera, S., Johnson, J., Kelly, D.P., Murrell, J.C., and H.Schäfer (2011c). Draft genome sequence of the chemolithoheterotrophic, halophilic methylotroph Methylophaga thiooxydans DMS010. J. Bact. 193, 3154-3155. DOI:10.1128/JB.00388-11.

Boden, R., Kelly, D. P., Murrell, J. C., and Schäfer, H (2010). Oxidation of dimethylsulfide to tetrathionate by Methylophaga thiooxidans sp. nov.: a new link in the sulfur cycle. Environmental Microbiology 12 (10), 2688-2699.

Charlson, R.J., Lovelock, J.E., Andreae, M.O., and Warren, S.G. (1987). Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature, 326, 655-661.

De Bont, J.A.M., van Dijken, J.P., and Harder, W. (1981). Dimethyl sulphoxide and dimethyl sulphide as a carbon, sulphur and energy source for growth of Hyphomicrobium S. J. Gen. Microbiol. 127, 315-323.

Eyice, Ö., Namura, M., Chen, Y., Mead, A., Samavedam, S., and H. Schäfer. 2015. SIP metagenomics identifies uncultivated Methylophilaceae as dimethylsulphide degrading bacteria in soil and lake sediment. ISME J, advance online publication, March 27, 2015; doi:10.1038/ismej.2015.37

Kiene, R.P. and T.S. Bates (1990). Biological removal of dimethyl sulfide from sea-water. Nature 345, 702-705.

Lidbury, I., Kröber, E., Zhang, Z., Zhu, Y., Murrell, J.C., Chen, Y., and H. Schäfer. 2016. A mechanism for bacterial transformation of DMS to DMSO: a missing link in the marine organic sulfur cycle. Environ. Microbiol. accepted. Online Early. DOI: 10.1111/1462-2920.13354

Schäfer, H. (2007). Isolation of Methylophaga spp. from marine dimethylsulfide-degrading enrichment cultures and identification of polypeptides induced during growth on dimethylsulfide. Appl. Environ. Microbiol. 73, 2580-2591.

Schäfer, H., Myronova, N. and Boden, R. (2010). Microbial degradation of dimethylsulfide and related C1-sulfur compounds: organisms and pathways controlling fluxes of sulfur in the biosphere' Journal Of Experimental Botany 61 (2), 315-334.


For more information, please contact: H.Schaefer@warwick.ac.uk