Dataset Information

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

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.

SUBMITTER: Li CY

PROVIDER: S-EPMC10356932 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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

Li Chun-Yang CY Cao Hai-Yan HY Wang Qing Q Carrión Ornella O Zhu Xiaoyu X Miao Jie J Wang Peng P Chen Xiu-Lan XL Todd Jonathan D JD Zhang Yu-Zhong YZ

The ISME journal 20230513 8

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 (H<sub>2</sub>S), a widely distributed and abundant volatile in natural environments, can be methylated to DMS. The microorganisms and the enzymes that convert H<sub>2</sub>S to DMS, and their importance in global sulfur cycling were unknown. Here w ...[more]

PMID: 37179443

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Project description:The sulfur-containing amino acid cysteine is abundant in the environment, including in freshwater lakes. Biological cysteine degradation can result in hydrogen sulfide (H2S), a toxic and ecologically relevant compound that is a central player in biogeochemical cycling in aquatic environments. Here, we investigated the ecological significance of cysteine in oxic freshwater, using isolated cultures, controlled experiments, and multiomics. We screened bacterial isolates enriched from natural lake water for their ability to produce H2S when provided cysteine. We identified 29 isolates (Bacteroidota, Proteobacteria, and Actinobacteria) that produced H2S. To understand the genomic and genetic basis for cysteine degradation and H2S production, we further characterized three isolates using whole-genome sequencing (using a combination of short-read and long-read sequencing) and tracked cysteine and H2S levels over their growth ranges: Stenotrophomonas maltophilia (Gammaproteobacteria), S. bentonitica (Gammaproteobacteria), and Chryseobacterium piscium (Bacteroidota). Cysteine decreased and H2S increased, and all three genomes had genes involved in cysteine degradation. Finally, to assess the presence of these organisms and genes in the environment, we surveyed a 5-year time series of metagenomic data from the same isolation source (Lake Mendota, Madison, WI, USA) and identified their presence throughout the time series. Overall, our study shows that diverse isolated bacterial strains can use cysteine and produce H2S under oxic conditions, and we show evidence using metagenomic data that this process may occur more broadly in natural freshwater lakes. Future considerations of sulfur cycling and biogeochemistry in oxic environments should account for H2S production from the degradation of organosulfur compounds. IMPORTANCE Hydrogen sulfide (H2S), a naturally occurring gas with both biological and abiotic origins, can be toxic to living organisms. In aquatic environments, H2S production typically originates from anoxic (lacking oxygen) environments, such as sediments, or the bottom layers of thermally stratified lakes. However, the degradation of sulfur-containing amino acids such as cysteine, which all cells and life forms rely on, can be a source of ammonia and H2S in the environment. Unlike other approaches for biological H2S production such as dissimilatory sulfate reduction, cysteine degradation can occur in the presence of oxygen. Yet, little is known about how cysteine degradation influences sulfur availability and cycling in freshwater lakes. In our study, we identified diverse bacteria from a freshwater lake that can produce H2S in the presence of O2. Our study highlights the ecological importance of oxic H2S production in natural ecosystems and necessitates a change in our outlook on sulfur biogeochemistry.

Dataset Information

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

Publications

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

Similar Datasets

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