Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri in an electric syntrophic coculture.

The direct conversion of CO2 to value-added chemical commodities, thereby storing solar energy, offers a promising option for alleviating both the current energy crisis and global warming. Semiconductor-biological hybrid systems are novel approaches. However, the inherent defects of photocorrosion, photodegradation, and the toxicity of the semiconductor limit the application of these biohybrid systems. We report here that Rhodopseudomonas palustris was able to directly act as a living photosensitizer to drive CO2 to CH4 conversion by Methanosarcina barkeri under illumination after coculturing. Specifically, R. palustris formed a direct electric syntrophic coculture with M. barkeri. Here, R. palustris harvested solar energy, performed anoxygenic photosynthesis using sodium thiosulfate as an electron donor, and transferred electrons extracellularly to M. barkeri to drive methane generation. The methanogenesis of M. barkeri in coculture was a light-dependent process with a production rate of 4.73 ± 0.23 µM/h under light, which is slightly higher than that of typical semiconductor-biohybrid systems (approximately 4.36 µM/h). Mechanistic and transcriptomic analyses showed that electrons were transferred either directly or indirectly (via electron shuttles), subsequently driving CH4 production. Our study suggests that R. palustris acts as a natural photosensitizer that, in coculture with M. barkeri, results in a new way to harvest solar energy that could potentially replace semiconductors in biohybrid systems.