The mosaic of aquatic photorespiration: evolution, diversity, and global biogeochemical impacts.

Aquatic phototrophs contribute over half of global carbon fixation, yet their photorespiratory metabolism remains a critical, underexplored component of the Earth's carbon cycle. First reported by Otto Warburg in the green alga Chlorella, Rubisco oxygenase activity produces the inhibitory metabolite 2-phosphoglycolate (2PG), requiring energetically demanding salvage pathways that release carbon and nitrogen. For decades, photorespiration in aquatic phototrophs was deemed negligible due to the widespread occurrence of CO2-concentrating mechanisms (CCMs) suppressing oxygenation. However, it is now clear that a basal yet essential photorespiratory flux persists even with active CCMs. This flux is dynamically regulated and integrated with central metabolism, rather than serving as a mere detoxification circuit. Across aquatic phototrophs, photorespiratory pathways exhibit remarkable diversity and lineage-specific subcellular organization, reflecting complex endosymbiotic histories and ecological adaptations. The photorespiratory intermediate glycolate can be excreted in many lineages, allowing the pathway to function as a metabolic safety valve that stabilizes redox poise under fluctuating conditions. At the ecosystem scale, glycolate excretion - approaching one gigaton of carbon annually - fuels heterotrophic microbial turnover and drives oceanic carbon cycling. Consequently, aquatic photorespiration emerges as a highly responsive process under environmental change and a dynamic hub within global biogeochemical fluxes.