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

Abstract

<p>Thiosulfate oxidation by microbes has a major impact on global sulfur cycling. Here, we provide evidence that bacteria within various <em>Roseobacter</em> lineages are important for thiosulfate oxidation in marine biofilms. We isolate and sequence the genomes of 54 biofilm-associated <em>Roseobacter</em> strains, finding conserved <em>sox</em> gene clusters for thiosulfate oxidation and plasmids, pointing to a niche-specific lifestyle. Analysis of global ocean metagenomic data suggests that <em>Roseobacter</em> 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 <em>sox</em> genes in biofilms belong to <em>Roseobacter</em> strains. Furthermore, we show that <em>Roseobacter</em> 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 <em>sox</em> gene expression and alterations in cell membrane protein composition, and promotes biofilm formation and anaerobic respiration. We propose that bacteria of the <em>Roseobacter</em> group are major thiosulfate-oxidizers in marine biofilms, where anaerobic thiosulfate metabolism is preferred.<br></p>