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Anaerobic thiosulfate oxidation by the Roseobacter group is prevalent in marine biofilms

Author

Listed:
  • Wei Ding

    (Ocean University of China
    The University of Hong Kong)

  • Shougang Wang

    (Ocean University of China)

  • Peng Qin

    (Ocean University of China)

  • Shen Fan

    (Ocean University of China)

  • Xiaoyan Su

    (Ocean University of China)

  • Peiyan Cai

    (The University of Hong Kong)

  • Jie Lu

    (Ocean University of China)

  • Han Cui

    (Ocean University of China)

  • Meng Wang

    (Ocean University of China)

  • Yi Shu

    (Ocean University of China)

  • Yongming Wang

    (Ocean University of China)

  • Hui-Hui Fu

    (Ocean University of China)

  • Yu-Zhong Zhang

    (Ocean University of China
    Shandong University)

  • Yong-Xin Li

    (The University of Hong Kong
    Southern Marine Science and Engineering Guangdong Laboratory)

  • Weipeng Zhang

    (Ocean University of China)

Abstract

Thiosulfate oxidation by microbes has a major impact on global sulfur cycling. Here, we provide evidence that bacteria within various Roseobacter lineages are important for thiosulfate oxidation in marine biofilms. We isolate and sequence the genomes of 54 biofilm-associated Roseobacter strains, finding conserved sox gene clusters for thiosulfate oxidation and plasmids, pointing to a niche-specific lifestyle. Analysis of global ocean metagenomic data suggests that Roseobacter strains are abundant in biofilms and mats on various substrates, including stones, artificial surfaces, plant roots, and hydrothermal vent chimneys. Metatranscriptomic analysis indicates that the majority of active sox genes in biofilms belong to Roseobacter strains. Furthermore, we show that Roseobacter strains can grow and oxidize thiosulfate to sulfate under both aerobic and anaerobic conditions. Transcriptomic and membrane proteomic analyses of biofilms formed by a representative strain indicate that thiosulfate induces sox gene expression and alterations in cell membrane protein composition, and promotes biofilm formation and anaerobic respiration. We propose that bacteria of the Roseobacter group are major thiosulfate-oxidizers in marine biofilms, where anaerobic thiosulfate metabolism is preferred.

Suggested Citation

  • Wei Ding & Shougang Wang & Peng Qin & Shen Fan & Xiaoyan Su & Peiyan Cai & Jie Lu & Han Cui & Meng Wang & Yi Shu & Yongming Wang & Hui-Hui Fu & Yu-Zhong Zhang & Yong-Xin Li & Weipeng Zhang, 2023. "Anaerobic thiosulfate oxidation by the Roseobacter group is prevalent in marine biofilms," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37759-4
    DOI: 10.1038/s41467-023-37759-4
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    References listed on IDEAS

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    1. Weipeng Zhang & Wei Ding & Yong-Xin Li & Chunkit Tam & Salim Bougouffa & Ruojun Wang & Bite Pei & Hoyin Chiang & Pokman Leung & Yanhong Lu & Jin Sun & He Fu & Vladimir B Bajic & Hongbin Liu & Nicole S, 2019. "Marine biofilms constitute a bank of hidden microbial diversity and functional potential," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    2. Chirag Jain & Luis M. Rodriguez-R & Adam M. Phillippy & Konstantinos T. Konstantinidis & Srinivas Aluru, 2018. "High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
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    5. Peter Menzel & Kim Lee Ng & Anders Krogh, 2016. "Fast and sensitive taxonomic classification for metagenomics with Kaiju," Nature Communications, Nature, vol. 7(1), pages 1-9, September.
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