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

Zhichao Zhou, Yang Liu, Jie Pan, Brandi R. Cron, Brandy M. Toner, Karthik Anantharaman, John A. Breier, Gregory J. Dick, Meng Li

Research output: Contribution to journalArticlepeer-review

41 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)3136-3148
Number of pages13
JournalISME Journal
Volume14
Issue number12
DOIs
StatePublished - Dec 1 2020

Bibliographical note

Publisher Copyright:
© 2020, The Author(s), under exclusive licence to International Society for Microbial Ecology.

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