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Aerobic methylation of hydrogen sulfide to dimethylsulfide in diverse microorganisms and environments

The ISME Journal volume 17, pages 1184–1193 (2023)Cite this article

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Abstract

Dimethylsulfide (DMS) is the major biosulfur source emitted to the atmosphere with key roles in global sulfur cycling and potentially climate regulation. The main precursor of DMS is thought to be dimethylsulfoniopropionate. However, hydrogen sulfide (H2S), a widely distributed and abundant volatile in natural environments, can be methylated to DMS. The microorganisms and the enzymes that convert H2S to DMS, and their importance in global sulfur cycling were unknown. Here we demonstrate that the bacterial MddA enzyme, previously known as a methanethiol S-methyltransferase, could methylate inorganic H2S to DMS. We determine key residues involved in MddA catalysis and propose the mechanism for H2S S-methylation. These results enabled subsequent identification of functional MddA enzymes in abundant haloarchaea and a diverse range of algae, thus expanding the significance of MddA mediated H2S methylation to other domains of life. Furthermore, we provide evidence for H2S S-methylation being a detoxification strategy in microorganisms. The mddA gene was abundant in diverse environments including marine sediments, lake sediments, hydrothermal vents and soils. Thus, the significance of MddA-driven methylation of inorganic H2S to global DMS production and sulfur cycling has likely been considerably underestimated.

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Fig. 1: Analyses of H2S S-methylation by environmental samples and microorganisms.
Fig. 2: Analyses of MddA enzymatic activities.
Fig. 3: Important PdMddA residues for enzymatic activity.
Fig. 4: The predicted catalytic mechanism of MddA and the enzymatic activities of MddA-like proteins in algae and archaea.
Fig. 5: MddA mediated H2S S-methylation in natural environments.
Fig. 6: Growth of N. sediminis and E. coli in response to H2S.

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Data availability

The predicted structure can be obtained from the AlphaFold Protein Structure Database (https://alphafold.ebi.ac.uk/) with accession code A0A0F6P9C0. The sequences of MddA and other proteins can be found in NCBI database as well as Supplementary Information files.

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Acknowledgements

We thank Terry McGenity from University of Essex for providing the Haladaptatus sp. W1 strain, and Emese Bartha from University of East Anglia for providing advice on how to culture it. This work was supported by the Marine S&T Fund of Shandong Province for Qingdao Marine Science and Technology Center (No. 2022QNLM030004-3), the National Key Research and Development Program of China (2022YFC2807500), the National Science Foundation of China (grants 42276102, 92251303, 42076229, 31961133016), the Fundamental Research Funds for the Central Universities (202172002, 202041011), the Major Scientific and Technological Innovation Project (MSTIP) of Shandong Province (2019JZZY010817), the Program of Shandong for Taishan Scholars (tspd20181203), the Biotechnology and Biological Sciences Research Council, UK, grant (BB/X005968), Natural Environment Research Council, UK, Standard grants (NE/X000990, NE/V000756 and NE/S001352) and the Leverhulme Trust research grant (RPG-2020-413).

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  1. These authors contributed equally: Chun-Yang Li, Hai-Yan Cao.

Authors and Affiliations

  1. MOE Key Laboratory of Evolution and Marine Biodiversity, Frontiers Science Center for Deep Ocean Multispheres and Earth System & College of Marine Life Sciences, Ocean University of China, Qingdao, China

    Chun-Yang Li, Hai-Yan Cao, Peng Wang & Yu-Zhong Zhang

  2. State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China

    Hai-Yan Cao, Qing Wang, Jie Miao, Xiu-Lan Chen & Yu-Zhong Zhang

  3. Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology, Qingdao, China

    Hai-Yan Cao, Peng Wang, Xiu-Lan Chen & Yu-Zhong Zhang

  4. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK

    Ornella Carrión, Xiaoyu Zhu & Jonathan D. Todd

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Contributions

CYL and YZZ designed and directed the research. JDT designed some experiments. HYC, CYL, QW, OC, XZ and JM performed the experiments. PW, XZ and XLC helped in data analysis. HYC, CYL, JDT and YZZ wrote the manuscript. XLC edited the manuscript.

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Correspondence to Hai-Yan Cao or Yu-Zhong Zhang.

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Li, CY., Cao, HY., Wang, Q. et al. Aerobic methylation of hydrogen sulfide to dimethylsulfide in diverse microorganisms and environments. ISME J 17, 1184–1193 (2023). https://doi.org/10.1038/s41396-023-01430-z

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