Electrosyntrophy drives anoxygenic photosynthetic bacteria to fix CO ₂ in the dark.

Anaerobes respire extracellular electron acceptors by extracellular electron transfer (EET). It is widely recognized that flavins can act as electron shuttles to facilitate this process. Flavin synthesis genes are widely distributed in Geobacter species. However, the functions of flavins in the EET of Geobacter species are unclear. Here, we demonstrate that G. uraniireducens can secrete abundant riboflavin (up to 270 nM) to facilitate EET. When an electrode was used as the electron acceptor, the quick recovery of anodizing current after anolyte replacement and the electrochemical behavior of the G. uraniireducens biofilm characterized by differential pulse voltammetry suggest that the self-secreted riboflavin promoted EET by serving as bound redox cofactors for cytochromes. On the contrary, when Fe(III) oxide was the electron acceptor, free riboflavin acted as electron shuttle to mediate the reduction of Fe(III) oxide. The results demonstrate the flexibility of flavins in EET, suggesting that the properties of electron acceptors can affect the binding mode of extracellular flavins, and broaden the knowledge of the EET of Geobacter species.

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.

Summary: Geobacter species can secrete free redox‐active flavins, but the role of these flavins in the interspecies electron transfer (IET) of Geobacter direct interspecies electron transfer (DIET) co‐culture is unknown. Here, we report the presence of a new riboflavin‐mediated interspecies electron transfer (RMIET) process in a traditional Geobacter DIET co‐culture; in this process, riboflavin contributes to IET by acting as a free‐form electron shuttle between free Geobacter species and serving as a bound cofactor of some cytochromes in Geobacter co‐culture aggregates. Multiple lines of evidence indicate that RMIET facilitates the primary initiation of syntrophic growth between Geobacter species before establishing the DIET co‐culture and provides additional ways alongside the DIET to transfer electrons to achieve electric syntrophy between Geobacter species. Redox kinetic analysis of riboflavin on either Geobacter species demonstrated that the Gmet_2896 cytochrome acts as the key riboflavin reduction site, while riboflavin oxidation by Geobacter sulfurreducens is the rate‐limiting step in RMIET, and the RMIET makes only a minor contribution to IET in Geobacter DIET co‐culture. The discovery of a new RMIET process in Geobacter DIET co‐culture suggests the complexity of IET in syntrophic bacterial communities and provides suggestions for the careful examination of the IET of other syntrophic co‐cultures.

The low power generation of microbial fuel cells limits their utility. Many factors can affect power generation, including inefficient electron transfer in the anode biofilm.