Abstract
Dimethylsulphoniopropionate (DMSP) accounts for up to 10% of carbon fixed by marine phytoplankton in ocean surface waters1,2, producing an estimated 11.7–103 Tmol S per year3, most of which is processed by marine bacteria through the demethylation/demethiolation pathway4. This pathway releases methanethiol (MeSH) instead of the climatically active gas dimethylsulphide (DMS) and enables marine microorganisms to assimilate the reduced sulphur5,6,7. Despite recognition of this critical microbial transformation for over two decades, the biochemical pathway and enzymes responsible have remained unidentified. Here we show that three new enzymes related to fatty acid β-oxidation constitute the pathway that assimilates methylmercaptopropionate (MMPA), the first product of DMSP demethylation/demethiolation, and that two previously unknown coenzyme A (CoA) derivatives, 3-methylmercaptopropionyl-CoA (MMPA-CoA) and methylthioacryloyl-CoA (MTA-CoA), are formed as novel intermediates. A member of the marine roseobacters, Ruegeria pomeroyi DSS-3, requires the MMPA-CoA pathway for MMPA assimilation and MeSH production. This pathway and the ability to produce MeSH from MMPA are present in diverse bacteria, and the ubiquitous SAR11 clade bacterium Pelagibacter ubique possesses enzymes for at least the first two steps. Analysis of marine metagenomic data indicates that the pathway is widespread among bacterioplankton in the ocean surface waters, making it one of the most important known routes for acquisition of reduced carbon and sulphur by surface ocean heterotrophs.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
Purchase on Springer Link
Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Archer, S. D., Widdicombe, C. E., Tarran, G. A., Rees, A. P. & Burkill, P. H. Production and turnover of particulate dimethylsulphoniopropionate during a coccolithophore bloom in the northern North Sea. Aquat. Microb. Ecol. 24, 225–241 (2001)
Simó, R., Archer, S. D., Pedros-Alio, C., Gilpin, L. & Stelfox-Widdicombe, C. E. Coupled dynamics of dimethylsulfoniopropionate and dimethylsulfide cycling and the microbial food web in surface waters of the North Atlantic. Limnol. Oceanogr. 47, 53–61 (2002)
Howard, E. C. et al. Bacterial taxa that limit sulfur flux from the ocean. Science 314, 649–652 (2006)
Kiene, R. P., Linn, L. J. & Bruton, J. A. New and important roles for DMSP in marine microbial communities. J. Sea Res. 43, 209–224 (2000)
van Duyl, F. C., Gieskes, W. W. C., Kop, A. J. & Lewis, W. E. Biological control of short-term variations in the concentration of DMSP and DMS during a Phaeocystis spring bloom. J. Sea Res. 40, 221–231 (1998)
Ledyard, K. M. & Dacey, J. W. H. Microbial cycling of DMSP and DMS in coastal and oligotrophic seawater. Limnol. Oceanogr. 41, 33–40 (1996)
Kiene, R. P., Linn, L. J., Gonzalez, J., Moran, M. A. & Bruton, J. A. Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl. Environ. Microbiol. 65, 4549–4558 (1999)
Andreae, M. O. Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Mar. Chem. 30, 1–29 (1990)
Charlson, R. J., Lovelock, J. E., Andreae, M. O. & Warren, S. G. Oceanic phytoplankton, atmospheric sulfur, cloud albedo and climate. Nature 326, 655–661 (1987)
Todd, J. D. et al. Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315, 666–669 (2007)
Curson, A. R. J., Rogers, R., Todd, J. D., Brearley, C. A. & Johnston, A. W. B. Molecular genetic analysis of a dimethylsulfoniopropionate lyase that liberates the climate-changing gas dimethylsulfide in several marine α-proteobacteria and Rhodobacter sphaeroides . Environ. Microbiol. 10, 1099 (2008)
Todd, J. D., Curson, A. R., Dupont, C. L., Nicholson, P. & Johnston, A. W. The dddP gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some Ascomycete fungi. Environ. Microbiol. 11, 1376–1385 (2009)
Todd, J. D. et al. DddQ, a novel, cupin-containing, dimethylsulfoniopropionate lyase in marine roseobacters and in uncultured marine bacteria. Environ. Microbiol. 13, 427–438 (2010)
Howard, E. C., Sun, S. L., Biers, E. J. & Moran, M. A. Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ. Microbiol. 10, 2397–2410 (2008)
Kiene, R. P. Production of methanethiol from dimethylsulfoniopropionate in marine surface waters. Mar. Chem. 54, 69–83 (1996)
Taylor, B. F. & Gilchrist, D. C. New routes for aerobic biodegradation of dimethylsulfoniopropionate. Appl. Environ. Microbiol. 57, 3581–3584 (1991)
Kiene, R. P. & Taylor, B. F. Demethylation of dimethylsulfoniopropionate and production of thiols in anoxic marine sediments. Appl. Environ. Microbiol. 54, 2208–2212 (1988)
Taylor, B. F. & Visscher, P. T. in Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds (eds Kiene, R. P., Kirst, G. O., Keller, M. D. & Visscher, P. T. ) Ch. 23, 265–276 (Springer-Verlag, 1996)
Bentley, R. & Chasteen, T. G. Environmental VOSCs–formation and degradation of dimethyl sulfide, methanethiol and related materials. Chemosphere 55, 291–317 (2004)
Tripp, H. J. et al. SAR11 marine bacteria require exogenous reduced sulphur for growth. Nature 452, 741–744 (2008)
Myers, R. W., Wray, J. W., Fish, S. & Abeles, R. H. Purification and characterization of an enzyme involved in oxidative carbon-carbon bond-cleavage reactions in the methionine salvage pathway of Klebsiella pneumoniae . J. Biol. Chem. 268, 24785–24791 (1993)
Gonzalez, J. M., Kiene, R. P. & Moran, M. A. Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the class Proteobacteria . Appl. Environ. Microbiol. 65, 3810–3819 (1999)
Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 5, e77 (2007)
Todd, J. D. et al. Molecular dissection of bacterial acrylate catabolism – unexpected links with dimethylsulfoniopropionate catabolism and dimethyl sulfide production. Environ. Microbiol. 12, 327–343 (2009)
Reisch, C. R., Moran, M. A. & Whitman, W. B. Dimethylsulfoniopropionate-dependent demethylase (DmdA) from Pelagibacter ubique and Silicibacter pomeroyi . J. Bacteriol. 190, 8018–8024 (2008)
Gonzalez, J. M. et al. Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int. J. Syst. Evol. Microbiol. 53, 1261–1269 (2003)
Deutsch, J., Grange, E., Rapoport, S. I. & Purdon, A. D. Isolation and quantitation of long-chain acyl-coenzyme-A esters in brain-tissue by solid-phase extraction. Anal. Biochem. 220, 321–323 (1994)
Venkateswaran, A. et al. Physiologic determinants of radiation resistance in Deinococcus radiodurans . Appl. Environ. Microbiol. 66, 2620–2626 (2000)
Bretscher, A. P. & Kaiser, D. Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J. Bacteriol. 133, 763–768 (1978)
Bell, R. P. & Higginson, W. C. E. The catalyzed dehydration of acetaldehyde hydrate, and the effect of structure on the velocity of protolytic reactions. Proc. R. Soc. Lond. A 197, 141–159 (1949)
Gupta, N. K. A study of formaldehyde dismutation by liver alcohol dehydrogenase with NAD+-analogs. Arch. Biochem. Biophys. 141, 632–640 (1970)
Stadtman, E. R. Preparation and assay of acyl coenzyme-A and other thiol esters - use of hydroxylamine. Methods Enzymol. 3, 931–941 (1957)
Chambers, S. T., Kunin, C. M., Miller, D. & Hamada, A. Dimethylthetin can substitute for glycine betaine as an osmoprotectant molecule for Escherichia coli . J. Bacteriol. 169, 4845–4847 (1987)
Li, M. Z. & Elledge, S. J. Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nature Methods 4, 251–256 (2007)
Henriksen, J. R. Physiology of dimethylsulfoniopropionate metabolism in a model marine Roseobacter, Silicibacter pomeroyi. PhD thesis, Univ. Georgia. (2008)
Keen, N. T., Tamaki, S., Kobayashi, D. & Trollinger, D. Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70, 191–197 (1988)
Koch, A. L. in Methods for general and molecular bacteriology (eds Gerhardt, P., Murray, R. G. E., Wood, W. A. & Krieg, N. R. ) 248–277 (American Society for Microbiology, 1994)
Neidhardt, F. C., Ingraham, J. L. & Schaechter, M. Physiology of the bacterial cell: a molecular approach. (Sinauer Associates, 1990)
Acknowledgements
We thank G. Wylie for assistance with NMR spectroscopy, S. Sharma, S. Sun and H. Luo for bioinformatics assistance, S. Gifford for technical advice, C. Smith and W. Crabb for technical assistance, and C. English for assistance with graphics. Funding for this research was provided by the National Science Foundation (MCB-0702125 and OCE-0724017) and the Gordon and Betty Moore Foundation.
Author information
Authors and Affiliations
Contributions
C.R.R. performed growth experiments, enzyme assays, protein purifications, substrate synthesis, phylogenetic analysis, and all reaction analysis except MALDI-FT-ICR. M.J.S. and I.J.A. performed MALDI-FT-ICR analysis. C.R.R. and V.A.V. performed genetic modifications of R. pomeroyi DSS-3. V.A.V. performed RT-qPCR. C.R.R. and M.A.M. conducted bioinformatic analyses. C.R.R., M.A.M. and W.B.W. designed the experiments and wrote the paper. All authors reviewed the manuscript before submission.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-10 with legends, Supplementary Tables 1-7 and an additional reference. (PDF 1455 kb)
PowerPoint slides
Rights and permissions
About this article
Cite this article
Reisch, C., Stoudemayer, M., Varaljay, V. et al. Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria. Nature 473, 208–211 (2011). https://doi.org/10.1038/nature10078
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature10078
This article is cited by
-
Strong chemotaxis by marine bacteria towards polysaccharides is enhanced by the abundant organosulfur compound DMSP
Nature Communications (2023)
-
Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater
Microbiome (2022)
-
Insights into methionine S-methylation in diverse organisms
Nature Communications (2022)
-
North Sea spring bloom-associated Gammaproteobacteria fill diverse heterotrophic niches
Environmental Microbiome (2021)
-
Sulfur metabolites in the pelagic ocean
Nature Reviews Microbiology (2019)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.