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

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 () and Weipeng Zhang ()
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Wei Ding: Ocean University of China
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
Yong-Xin Li: The University of Hong Kong
Weipeng Zhang: Ocean University of China

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-37759-4

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