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Metagenomic analysis reveals wide distribution of phototrophic bacteria in hydrothermal vents on the ultraslow-spreading Southwest Indian Ridge

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Abstract

Deep-sea hydrothermal vents are known as chemosynthetic ecosystems. However, high temperature vents emit light that hypothetically can drive photosynthesis in this habitat. Metagenomic studies have sporadically reported the occurrence of phototrophic populations such as cyanobacteria in hydrothermal vents. To determine how geographically and taxonomically widespread phototrophs are in deep-sea hydrothermal vents, we collected samples from three niches in a hydrothermal vent on the Southwest Indian Ridge and carried out an integrated metagenomic analysis. We determined the typical community structures of microorganisms found in active venting fields and identified populations of known potential chlorophototrophs and retinalophototrophs. Complete chlorophyll biosynthetic pathways were identified in all samples. By contrast, proteorhodopsins were only found in active beehive smoker diffusers. Taxonomic groups possessing potential phototrophy dependent on semiconductors present in hydrothermal vents were also found in these samples. This systematic comparative metagenomic study reveals the widespread distribution of phototrophic bacteria in hydrothermal vent fields. Our results support the hypothesis that the ocean is a seed bank of diverse microorganisms. Geothermal vent light may provide energy and confer a competitive advantage on phototrophs to proliferate in hydrothermal vent ecosystems.

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Data availability

The data that support the findings of this study have been deposited into CNGB Sequence Archive (CNSA)(Guo et al. 2020) of China National GeneBank DataBase (CNGBdb)(Chen et al. 2020) with accession number CNP0002004. All data are available. The nucleotide sequence data reported are available in the GenBank database under accession numbers MW133229, MW133230, MW133231, MW133232, and MZ351491.

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (No. 2018YFC0309904), the National Natural Science Foundation of China (Nos. 91751202, 41806174, 91751108), the Key Research and Development Program of Hainan Province (No. ZDKJ2019011), Grant Y9719105 from the Institute of Deep-sea Technology Innovation, Chinese Academy of Sciences (IDSTI-CAS), Grant 2019YD16 from Sanya City and Grant INSB-DBM2021 and support to LIA-MagMC from Centre National de la Recherche Scientifique. We thank cruise members of expedition TS10 of the R/V TSYH, especially the pilots of the manned submersible ShenHaiYongShi and Y Lu, YW Pan and VH Pellizari for assistance in sampling.

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Author notes

  1. Hong Chen and Deng Hui Li contributed equally.

Authors and Affiliations

  1. Laboratory of Deep Sea Microbial Cell Biology, Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, 572000, China

    Hong Chen, Xue Gong Li, Xiao Qing Qi, Jie Dai, Rui Zhao & Wei-Jia Zhang

  2. University of Chinese Academy of Sciences, Beijing, 100864, China

    Hong Chen, Jie Dai & Rui Zhao

  3. France-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms (LIA-MagMC), Marseille, France/Sanya, China

    Hong Chen, Xue Gong Li, Xiao Qing Qi, Jie Dai, Rui Zhao, Wei-Jia Zhang & Long-Fei Wu

  4. Institution of Deep-Sea Life Sciences, IDSSE-BGI, IDSTI-CAS/Hainan Deep-Sea Technology Laboratory, Sanya/Shenzhen, China

    Hong Chen, Deng Hui Li, Ai Jun Jiang, Xue Gong Li, Jian Wei Chen, Xiao Qing Qi, Jie Dai, Rui Zhao, Wei-Jia Zhang & Shan Shan Liu

  5. BGI-Qingdao, BGI-Shenzhen, Qingdao, 266555, China

    Deng Hui Li, Ai Jun Jiang, Jian Wei Chen & Shan Shan Liu

  6. Zhejiang University, Hangzhou, 310027, China

    Shi Jun Wu & Meng Jie Qu

  7. BGI-Shenzhen, Shenzhen, 518083, China

    Jian Wei Chen & Shan Shan Liu

  8. Qingdao-Europe Advanced Institute for Life Sciences, BGI-Shenzhen, Qingdao, 266555, China

    Jian Wei Chen & Shan Shan Liu

  9. Aix Marseille University, Centre national de la recherche scientifique, Laboratoire de Chimie Bactérienne, Institut de Microbiologie de la Méditerranée, L’ Institut Microbiologie, Bioénergies et Biotechnologie, 13402, Marseille, France

    Long-Fei Wu

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  1. Hong Chen
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Contributions

HC, performed research, analyzed data, prepared figures; DHL, analyzed data, wrote the paper; AJJ, performed research; XGL, analyzed data; SJW, performed research; JWC, analyzed data, wrote the paper; MJQ, performed research; XQQ, analyzed data; JD, analyzed data; RZ, analyzed data; WJZ, analyzed data, wrote the paper; SSL, analyzed data; LFW, conceived of and designed study, performed research, analyzed data, wrote the paper.

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Correspondence to Wei-Jia Zhang or Long-Fei Wu.

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There are no conflicts of interest or competing interests.

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No human or animal materials were used in this study.

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Edited by Chengchao Chen.

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Chen, H., Li, D.H., Jiang, A.J. et al. Metagenomic analysis reveals wide distribution of phototrophic bacteria in hydrothermal vents on the ultraslow-spreading Southwest Indian Ridge. Mar Life Sci Technol 4, 255–267 (2022). https://doi.org/10.1007/s42995-021-00121-y

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