Metagenomic insights into the functions of microbial communities in sulfur-rich sediment of a shallow-water hydrothermal vent off Kueishan Island

Li Wang; Ziyi Shen; Xinyi Cheng; Jiang-Shiou Hwang; Yizhe Guo; Mingye Sun; Junwei Cao; Rulong Liu; Jiasong Fang

doi:10.3389/fmicb.2022.992034

Metagenomic insights into the functions of microbial communities in sulfur-rich sediment of a shallow-water hydrothermal vent off Kueishan Island

Front Microbiol. 2022 Nov 30:13:992034. doi: 10.3389/fmicb.2022.992034. eCollection 2022.

Authors

Li Wang¹, Ziyi Shen¹, Xinyi Cheng¹, Jiang-Shiou Hwang², Yizhe Guo¹, Mingye Sun¹, Junwei Cao¹, Rulong Liu¹, Jiasong Fang^{1

3}

Affiliations

¹ Shanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, China.
² Institute of Marine Biology, National Taiwan Ocean University, Keelung, Taiwan.
³ Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China.

Abstract

Hydrothermal vent (HTV) systems are important habitats for understanding the biological processes of extremophiles on Earth and their relative contributions to material and energy cycles in the ocean. Current understanding on hydrothermal systems have been primarily focused on deep-sea HTVs, and little is known about the functions and metabolisms of microorganisms in shallow-water HTVs (SW-HTVs), which are distinguished from deep-sea HTVs by a depth limit of 200 m. In this study, we analyzed metagenomes of sulfur-rich sediment samples collected from a SW-HTV of Kueishan Island, located in a marginal sea of the western Pacific Ocean. Comparing with a previously published report of pelagic samples from the nearby sampling site, microbial communities in the SW-HTV sediments enriching with genes of both aerobic and anaerobic respiration inferred variable environments in the tested sediments. Abundant genes of energy metabolism encoding sulfur oxidation, H₂ oxidation, and carbon fixation were detected from the sediment samples. Sixty-eight metagenome-assembled-genomes (MAGs) were reconstructed to further understand the metabolism and potential interactions between different microbial taxa in the SW-HTVs sediment. MAGs with the highest abundant were chemolithotrophic sulfur-oxidization bacteria, including Sulfurovum represented Campylobacteria involved sox multienzyme, sulfide oxidation genes and rTCA cycle, and Gammaproteobacteria involved dsr gene and CBB cycle. In addition, Desulfobacterota with the potential to participate in sulfur-disproportionating processes also had higher abundance than the sample's overall mean value. The interaction of these bacterial groups allows the microbial communities to efficiently metabolize a large variety of sulfur compounds. In addition, the potential to use simple organic carbon, such as acetate, was found in chemolithotrophic Campylobacterial MAGs. Collectively, our results revealed the complexity of environmental conditions of the vent sediment and highlight the interactive relationships of the dominant microbial populations in driving sulfur cycles in the SW-HTV sediments off Kueishan Island.

Keywords: Campylobacteria; Kueishan Island; metagenome-assembled-genomes; sediment; shallow-water hydrothermal vent; sulfur cycle.