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The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol

Nature Microbiology volume 1, Article number: 16065 (2016) Cite this article

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A Corrigendum to this article was published on 03 October 2016

Abstract

Marine phytoplankton produce ∼109 tonnes of dimethylsulfoniopropionate (DMSP) per year1,2, an estimated 10% of which is catabolized by bacteria through the DMSP cleavage pathway to the climatically active gas dimethyl sulfide3,4. SAR11 Alphaproteobacteria (order Pelagibacterales), the most abundant chemo-organotrophic bacteria in the oceans, have been shown to assimilate DMSP into biomass, thereby supplying this cell's unusual requirement for reduced sulfur5,6. Here, we report that Pelagibacter HTCC1062 produces the gas methanethiol, and that a second DMSP catabolic pathway, mediated by a cupin-like DMSP lyase, DddK, simultaneously shunts as much as 59% of DMSP uptake to dimethyl sulfide production. We propose a model in which the allocation of DMSP between these pathways is kinetically controlled to release increasing amounts of dimethyl sulfide as the supply of DMSP exceeds cellular sulfur demands for biosynthesis.

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Figure 1: DMSP metabolism in HTCC1062.
Figure 2: Production of gaseous DMSP products as cells accumulate intracellular DMSP.
Figure 3: DMSP catabolic pathways and homologues identified in HTCC1062.

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Acknowledgements

The authors thank J.W.H. Dacey for providing DMSP and E. Boss for help with modelling the transport kinetics. The authors thank J.W.H. Dacey and S. Bennett for advice regarding the methods for DMSP measurements and N. Le Brun for suggestions on the properties of the cupin lyases and kinetics analysis. J.S. acknowledges China Scholarships Council (CSC) for financial support. Major support was provided by a grant from the Marine Microbiology Initiative of the Gordon and Betty Moore Foundation (grant no. GBMF607.01 to S.J.G.). Proteomics measurements were supported by the US Department of Energy's (DOE) Office of Biological and Environmental Research (OBER) Pan-omics programme at Pacific Northwest National Laboratory (PNNL) and performed in the Environmental Molecular Sciences Laboratory, a DOE OBER national scientific user facility on the PNNL campus. A.W.B.J. and J.D.T. were supported by grant no. NE/H008586/1 from the UK Natural Environment Research Council and E.K.F. was supported by a studentship from the Tyndall Centre at the University of East Anglia. Funds for the PTR-TOF were provided by NASA (grant no. NNX15AE70G to K.H.H. and S.J.G.) and by a grant to K.H.H. from the Oregon State University Research Office. This research was supported by the US National Science Foundation (grant OCE-1436865).

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Authors and Affiliations

  1. Department of Microbiology, Oregon State University, Corvallis, 97331, Oregon, USA

    Jing Sun, Cleo L. Davie-Martin, Kimberly H. Halsey & Stephen J. Giovannoni

  2. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK

    Jonathan D. Todd, Emily K. Fowler & Andrew W.B. Johnston

  3. Department of Biological Sciences, Louisiana State University, Baton Rouge, 70803, Louisiana, USA

    J. Cameron Thrash

  4. Department of Food Science, Oregon State University, Corvallis, 97331, Oregon, USA

    Yanping Qian & Michael C. Qian

  5. Department of Biosciences, University of Exeter, Exeter, EX4 4QD, UK

    Ben Temperton

  6. Qingdao Aquarium, Qingdao, 266003, Shandong, China

    Jiazhen Guo

  7. Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, 99352, Washington, USA

    Joshua T. Aldrich, Carrie D. Nicora, Mary S. Lipton, Richard D. Smith & Samuel H. Payne

  8. Department of Mathematics, Oregon State University, Corvallis, 97331, Oregon, USA

    Patrick De Leenheer

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Contributions

J.S. and S.J.G. conceived and designed the experiments. J.S., Y.Q. and M.C.Q. measured DMSP products and intracellular DMSP concentration. J.S. and J.G. performed the physiological growth experiments for HTCC1062. J.S. and J.C.T. analysed and proposed DMSP metabolic pathways. J.D.T., E.K.F. and A.W.B.J. designed and implemented the cloning, expression and characterization of DddK. B.T. performed metagenomics analyses. B.T., J.T.A., C.D.N., M.S.L., R.D.S. and S.H.P. performed iTRAQ and data analyses. P.D.L. and S.J.G. proposed the model. C.L.D.-M. and K.H.H. measured real-time DMS/MeSH production by PTR-TOF/MS. S.J.G. contributed reagents, materials and analysis tools.

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Correspondence to Stephen J. Giovannoni.

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The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary Notes I-V, Supplementary Figures 1-9, Supplementary Tables 1-3, Supplementary Table 4 Legend, Supplementary Methods and Supplementary References (PDF 1476 kb)

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Sun, J., Todd, J., Thrash, J. et al. The abundant marine bacterium Pelagibacter simultaneously catabolizes dimethylsulfoniopropionate to the gases dimethyl sulfide and methanethiol. Nat Microbiol 1, 16065 (2016). https://doi.org/10.1038/nmicrobiol.2016.65

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