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Gammaproteobacteria mediating utilization of methyl-, sulfur- and petroleum organic compounds in deep ocean hydrothermal plumes

Abstract

Deep-sea hydrothermal plumes are considered natural laboratories for understanding ecological and biogeochemical interactions. Previous studies focused on interactions between microorganisms and inorganic, reduced hydrothermal inputs including sulfur, hydrogen, iron, and manganese. However, little is known about transformations of organic compounds, especially methylated, sulfur-containing compounds, and petroleum hydrocarbons. Here, we reconstructed nine gammaproteobacterial metagenome-assembled genomes, affiliated with Methylococcales, Methylophaga, and Cycloclasticus, from three hydrothermal ecosystems. We present evidence that these three groups have high transcriptional activities of genes encoding cycling of C1-compounds, petroleum hydrocarbons, and organic sulfur in hydrothermal plumes. This includes oxidation of methanethiol, the simplest thermochemically-derived organic sulfur, for energy metabolism in Methylococcales and Cycloclasticus. Together with active transcription of genes for thiosulfate and methane oxidation in Methylococcales, these results suggest an adaptive strategy of versatile and simultaneous use of multiple available electron donors. Meanwhile, the first near-complete MAG of hydrothermal Methylophaga aminisulfidivorans and its transcriptional profile point to active chemotaxis targeting small organic compounds. Petroleum hydrocarbon-degrading Cycloclasticus are abundant and active in plumes of oil spills as well as deep-sea vents, suggesting that they are indigenous and effectively respond to stimulus of hydrocarbons in the deep sea. These findings suggest that these three groups of Gammaproteobacteria transform organic carbon and sulfur compounds via versatile and opportunistic metabolism and modulate biogeochemistry in plumes of hydrothermal systems as well as oil spills, thus contributing broad ecological impact to the deep ocean globally.

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Fig. 1: Phylogenetic tree of the hydrothermal plume and background MAGs based on concatenated marker proteins.
Fig. 2: Genomic, phylogenetic, and transcriptomic analyses of mto genes.
Fig. 3: The metabolism of Methylophaga aminisulidivorans SZUA-1124.
Fig. 4: Schematic figure indicating ecology and function of Hydro-γ-MAGs.

Data availability

The Sequence Read Archive IDs for metagenomic and metatranscriptomic are summarized in Supplementary Dataset S3. The MAGs that were resolved from this study are deposited under NCBI BioProject PRJNA488180. The further analyses on gene operons of methyl-metabolism, transcriptomic ratio of Hydro-γ-MAGs, and Cycloclasticus expression in DWH are present in Supplementary Information and Figs. S11S18.

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Acknowledgements

Thanks to the suggestions and critical reviews from anonymous reviewers. Thanks to the proofreading efforts and comments from Patricia Tran from University of Wisconsin – Madison. This study was funded by National Natural Science Foundation of China (No. 91851105, 31970105), the Science and Technology Innovation Committee of Shenzhen (No. JCYJ20170818091727570), the Key Project of Department of Education of Guangdong Province (No. 2017KZDXM071), Gordon and Betty Moore Foundation (GBMF2609 to GJD), and the National Science Foundation (OCE 1029242). We are grateful to the captains, crew, and chief scientists (Fred Prahl, Brian Popp, Anna-Louise Reysenbach, and Chris German) of the cruises on which samples were collected.

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Zhou, Z., Liu, Y., Pan, J. et al. Gammaproteobacteria mediating utilization of methyl-, sulfur- and petroleum organic compounds in deep ocean hydrothermal plumes. ISME J 14, 3136–3148 (2020). https://doi.org/10.1038/s41396-020-00745-5

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