Quantitative proteomics reveals the Sox system's role in sulphur and arsenic metabolism of phototroph Halorhodospira halophila

Abstract

The metabolic process of purple sulphur bacteria's anoxygenic photosynthesis has been primarily studied in Allochromatium vinosum, a member of the Chromatiaceae family. However, the metabolic processes of purple sulphur bacteria from the Ectothiorhodospiraceae and Halorhodospiraceae families remain unexplored. We have analysed the proteome of Halorhodospira halophila, a member of the Halorhodospiraceae family, which was cultivated with various sulphur compounds. This analysis allowed us to reconstruct the first comprehensive sulphur-oxidative photosynthetic network for this family. Some members of the Ectothiorhodospiraceae family have been shown to use arsenite as a photosynthetic electron donor. Therefore, we analysed the proteome response of Halorhodospira halophila when grown under arsenite and sulphide conditions. Our analyses using ion chromatography-inductively coupled plasma mass spectrometry showed that thioarsenates are chemically formed under these conditions. However, they are more extensively generated and converted in the presence of bacteria, suggesting a biological process. Our quantitative proteomics revealed that the SoxAXYZB system, typically dedicated to thiosulphate oxidation, is overproduced under these growth conditions. Additionally, two electron carriers, cytochrome c₅₅₁/c₅ and HiPIP III, are also overproduced. Electron paramagnetic resonance spectroscopy suggested that these transporters participate in the reduction of the photosynthetic Reaction Centre. These results support the idea of a chemically and biologically formed thioarsenate being oxidized by the Sox system, with cytochrome c₅₅₁/c₅ and HiPIP III directing electrons towards the Reaction Centre.