Committee: Yoichi Kamagata, Ryoma Kamikawa, Yoshitomo Kikuchi, Atsushi Kouzuma, Shusei Sato, Shino Suzuki (Chair), and Fumito Maruyama (Names listed without honorifics)

Syntrophic Interaction between an Anoxygenic Photosynthetic Bacterium and a Tetrathionate-reducing Bacterium in Anaerobic Benzoate Degradation.

Microbes and Environments, 2025, Volume 40, Issue 1, Article ID: ME24105

Miao He, Shin-ichi Nishitani, Shin Haruta

Reason for the Award

This study demonstrated that anaerobic benzoate degradation under illuminated conditions is enabled by a syntrophic metabolic interaction between the purple sulfur bacterium Marichromatium sp. strain PS1, isolated from marine sediment, and the non-phototrophic bacterium Marinobacterium sp. strain BA1. Strain PS1 oxidizes thiosulfate (S₂O₃²⁻) as an electron donor for photosynthesis, producing sulfate and tetrathionate (S₄O₆²⁻). In turn, strain BA1 uses reducing power generated through benzoate oxidation to reduce tetrathionate back to thiosulfate, while also supplying strain PS1 with carbon dioxide produced during benzoate oxidation. Through this bidirectional exchange of carbon and sulfur compounds, the authors proposed a model in which the metabolisms of phototrophic and heterotrophic microorganisms are coupled through a redox cycle between thiosulfate and tetrathionate.In studies of microbial energy metabolism involving sulfur compounds, hydrogen sulfide, elemental sulfur, and sulfate have traditionally been regarded as major electron donors or acceptors. In contrast, this study is highly novel in demonstrating that electron transfer between thiosulfate and tetrathionate can couple photosynthesis with anaerobic degradation of aromatic compounds. The metabolic model was supported from multiple perspectives by combining comparisons of pure and co-cultures, quantitative measurements of benzoate and various sulfur compounds, analyses of microbial growth, and genome analysis. By examining microbial function in the context of interspecies interactions and environmental biogeochemical cycling, this work strongly exemplifies the distinctive scope and scientific vision of Microbes and Environments.Future transcriptomic comparisons between mono- and co-cultures are expected to identify genes that respond to metabolite exchange between the two strains and to clarify the pathway responsible for anaerobic benzoate degradation in strain BA1. It will also be important to determine how widely environments capable of generating and sustaining both thiosulfate and tetrathionate occur in natural marine sediments, particularly at redox interfaces, in illuminated but oxygen-limited surface sediments, and in settings where aromatic compounds such as benzoate are supplied. Further investigations at both the molecular and environmental levels will help establish the generality of the syntrophic interaction identified in this study and clarify its ecological significance for marine carbon and sulfur cycling.In summary, this study presents a novel mechanism by which carbon and sulfur metabolism are linked in marine sediments through a syntrophic interaction between a phototrophic microorganism and a heterotrophic microorganism. Its originality, conceptual significance, and strong potential for further development make it highly deserving of the Paper Award.