Biophotoelectrochemical process co-driven by dead microalgae and live bacteria

Abstract

Anaerobic reduction processes in natural waters can be promoted by dead microalgae that have been attributed to nutrient substances provided by the decomposition of dead microalgae for other microorganisms. However, previous reports have not considered that dead microalgae may also serve as photosensitizers to drive microbial reduction processes. Here we demonstrate a photoelectric synergistic linkage between dead microalgae and bacteria capable of extracellular electron transfer (EET). Illumination of dead Raphidocelis subcapitata resulted in two-fold increase in the rate of anaerobic bioreduction by pure Geobacter sulfurreducens, suggesting that photoelectrons generated from the illuminated dead microalgae were transferred to the EET-capable microorganisms. Similar phenomena were observed in NO₃^- reduction driven by irradiated dead Chlorella vulgaris and living Shewanella oneidensis, and Cr(VI) reduction driven by irradiated dead Raphidocelis subcapitata and living Bacillus subtilis. Enhancement of bioreduction was also seen when the killed microalgae were illuminated in mixed-culture lake water, suggesting that EET-capable bacteria were naturally present and this phenomenon is common in post-bloom systems. The intracellular ferredoxin-NADP⁺-reductase is inactivated in the dead microalgae, allowing the production and extracellular transfer of photoelectrons. The use of mutant strains confirmed that the electron transport pathway requires multiheme cytochromes. Taken together, these results suggest a heretofore overlooked biophotoelectrochemical process jointly mediated by illumination of dead microalgae and live EET-capable bacteria in natural ecosystems, which may add an important component in the energetics of bioreduction phenomena particularly in microalgae-enriched environments.