Dataset Information

Metagenomic Insights Into the Cycling of Dimethylsulfoniopropionate and Related Molecules in the Eastern China Marginal Seas.

ABSTRACT: The microbial cycling of dimethylsulfoniopropionate (DMSP) and its gaseous catabolites dimethylsulfide (DMS) and methanethiol (MeSH) are important processes in the global sulfur cycle, marine microbial food webs, signaling pathways, atmospheric chemistry, and potentially climate regulation. Many functional genes have been identified and used to study the genetic potential of microbes to produce and catabolize these organosulfur compounds in different marine environments. Here, we sampled seawater, marine sediment and hydrothermal sediment, and polymetallic sulfide in the eastern Chinese marginal seas and analyzed their microbial communities for the genetic potential to cycle DMSP, DMS, and MeSH using metagenomics. DMSP was abundant in all sediment samples, but was fivefold less prominent in those from hydrothermal samples. Indeed, Yellow Sea (YS) sediment samples had DMSP concentrations two orders of magnitude higher than in surface water samples. Bacterial genetic potential to synthesize DMSP (mainly in Rhodobacteraceae bacteria) was far higher than for phytoplankton in all samples, but particularly in the sediment where no algal DMSP synthesis genes were detected. Thus, we propose bacteria as important DMSP producers in these marine sediments. DMSP catabolic pathways mediated by the DMSP lyase DddP (prominent in Pseudomonas and Mesorhizobium bacteria) and DMSP demethylase DmdA enzymes (prominent in Rhodobacteraceae bacteria) and MddA-mediated MeSH S-methylation were very abundant in Bohai Sea and Yellow Sea sediments (BYSS) samples. In contrast, the genetic potential for DMSP degradation was very low in the hydrothermal sediment samples-dddP was the only catabolic gene detected and in only one sample. However, the potential for DMS production from MeSH (mddA) and DMS oxidation (dmoA and ddhA) was relatively abundant. This metagenomics study does not provide conclusive evidence for DMSP cycling; however, it does highlight the potential importance of bacteria in the synthesis and catabolism of DMSP and related compounds in diverse sediment environments.

SUBMITTER: Song D

PROVIDER: S-EPMC7039863 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Metagenomic Insights Into the Cycling of Dimethylsulfoniopropionate and Related Molecules in the Eastern China Marginal Seas.

Song Delei D Zhang Yunhui Y Liu Ji J Zhong Haohui H Zheng Yanfen Y Zhou Shun S Yu Min M Todd Jonathan D JD Zhang Xiao-Hua XH

Frontiers in microbiology 20200218

The microbial cycling of dimethylsulfoniopropionate (DMSP) and its gaseous catabolites dimethylsulfide (DMS) and methanethiol (MeSH) are important processes in the global sulfur cycle, marine microbial food webs, signaling pathways, atmospheric chemistry, and potentially climate regulation. Many functional genes have been identified and used to study the genetic potential of microbes to produce and catabolize these organosulfur compounds in different marine environments. Here, we sampled seawate ...[more]

PMID: 32132981

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Project description:Dimethylsulfoniopropionate (DMSP) and related organic sulfur compounds play key roles in global sulfur cycling. Bacteria have been found to be important DMSP producers in seawater and surface sediments of the aphotic Mariana Trench (MT). However, detailed bacterial DMSP cycling in the Mariana Trench subseafloor remains largely unknown. Here, the bacterial DMSP-cycling potential in a Mariana Trench sediment core (7.5 m in length) obtained at a 10,816-m water depth was investigated using culture-dependent and -independent methods. The DMSP content fluctuated along the sediment depth and reached the highest concentration at 15 to 18 cm below the seafloor (cmbsf). dsyB was the dominant known DMSP synthetic gene, existing in 0.36 to 1.19% of the bacteria, and was identified in the metagenome-assembled genomes (MAGs) of previously unknown bacterial DMSP synthetic groups such as Acidimicrobiia, Phycisphaerae, and Hydrogenedentia. dddP, dmdA, and dddX were the major DMSP catabolic genes. The DMSP catabolic activities of DddP and DddX retrieved from Anaerolineales MAGs were confirmed by heterologous expression, indicating that such anaerobic bacteria might participate in DMSP catabolism. Moreover, genes involved in methanethiol (MeSH) production from methylmercaptopropionate (MMPA) and dimethyl sulfide (DMS), MeSH oxidation, and DMS production were highly abundant, suggesting active conversions between different organic sulfur compounds. Finally, most culturable DMSP synthetic and catabolic isolates possessed no known DMSP synthetic and catabolic genes, and actinomycetes could be important groups involved in both DMSP synthesis and catabolism in Mariana Trench sediment. This study extends the current understanding of DMSP cycling in Mariana Trench sediment and highlights the need to uncover novel DMSP metabolic genes/pathways in extreme environments. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is an abundant organosulfur molecule in the ocean and is the precursor for the climate-active volatile gas dimethyl sulfide. Previous studies focused mainly on bacterial DMSP cycling in seawater, coastal sediment, and surface trench sediment samples, but DMSP metabolism in the Mariana Trench (MT) subseafloor sediments remains unknown. Here, we describe the DMSP content and metabolic bacterial groups in the subseafloor of the MT sediment. We found that the tendency for vertical variation of the DMSP content in the MT was distinct from that of the continent shelf sediment. Although dsyB and dddP were the dominant DMSP synthetic and catabolic genes in the MT sediment, respectively, both metagenomic and culture methods revealed multiple previously unknown DMSP metabolic bacterial groups, especially anaerobic bacteria and actinomycetes. The active conversion of DMSP, DMS, and methanethiol may also occur in the MT sediments. These results provide novel insights for understanding DMSP cycling in the MT.

Project description:BackgroundDimethyl sulfide (DMS) is the dominant volatile organic sulfur in global oceans. The predominant source of oceanic DMS is the cleavage of dimethylsulfoniopropionate (DMSP), which can be produced by marine bacteria and phytoplankton. Polar oceans, which represent about one fifth of Earth's surface, contribute significantly to the global oceanic DMS sea-air flux. However, a global overview of DMS and DMSP cycling in polar oceans is still lacking and the key genes and the microbial assemblages involved in DMSP/DMS transformation remain to be fully unveiled.ResultsHere, we systematically investigated the biogeographic traits of 16 key microbial enzymes involved in DMS/DMSP cycling in 60 metagenomic samples from polar waters, together with 174 metagenome and 151 metatranscriptomes from non-polar Tara Ocean dataset. Our analyses suggest that intense DMS/DMSP cycling occurs in the polar oceans. DMSP demethylase (DmdA), DMSP lyases (DddD, DddP, and DddK), and trimethylamine monooxygenase (Tmm, which oxidizes DMS to dimethylsulfoxide) were the most prevalent bacterial genes involved in global DMS/DMSP cycling. Alphaproteobacteria (Pelagibacterales) and Gammaproteobacteria appear to play prominent roles in DMS/DMSP cycling in polar oceans. The phenomenon that multiple DMS/DMSP cycling genes co-occurred in the same bacterial genome was also observed in metagenome assembled genomes (MAGs) from polar oceans. The microbial assemblages from the polar oceans were significantly correlated with water depth rather than geographic distance, suggesting the differences of habitats between surface and deep waters rather than dispersal limitation are the key factors shaping microbial assemblages involved in DMS/DMSP cycling in polar oceans.ConclusionsOverall, this study provides a global overview of the biogeographic traits of known bacterial genes involved in DMS/DMSP cycling from the Arctic and Antarctic oceans, laying a solid foundation for further studies of DMS/DMSP cycling in polar ocean microbiome at the enzymatic, metabolic, and processual levels. Video Abstract.

Dataset Information

Metagenomic Insights Into the Cycling of Dimethylsulfoniopropionate and Related Molecules in the Eastern China Marginal Seas.

Publications

Metagenomic Insights Into the Cycling of Dimethylsulfoniopropionate and Related Molecules in the Eastern China Marginal Seas.

Similar Datasets

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