Extracellular electron transport in coral-algal symbiosis studied by chlorophyll fluorescence relaxation and ferricyanide reduction

Abstract

Coral health depends on intricate metabolic interactions between the coral host and its symbiotic algae, Symbiodiniaceae. While nutrient exchange is well established, electron-level interactions have remained unexplored. Here, we provide evidence for extracellular electron transport (EET) within coral-algal symbiosis, supported by variable chlorophyll (Chl) fluorescence and ferricyanide reduction measurements. We observed a slow wave in the relaxation of flash-induced Chl fluorescence kinetics under microaerobic conditions in both isolated Fugacium kawagutii (CS156) cells and intact corals, reflecting redox dynamics of the primary quinone electron acceptor (QA) in the photosynthetic electron transport chain. The addition of the extracellular electron acceptor ferricyanide decreased the wave amplitude and QA reduction while being reduced to ferrocyanide, demonstrating EET from the symbiont to extracellular acceptors. Slower Chl fluorescence rise kinetics under continuous illumination in intact corals compared to isolated symbionts indicate that electrons may also flow from symbionts to the host. Under low oxygen conditions, QA was gradually reduced in corals in darkness but not in isolated symbiont cultures, suggesting electron transfer from host to symbiont. Together, these results indicate bidirectional extracellular electron exchange between symbiotic partners, pointing to a previously unrecognized mechanism for redox balancing in coral-algal symbiosis. This pathway likely contributes to metabolic resilience and the maintenance of coral health under fluctuating environmental conditions.