Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection

All colonial diazotrophic cyanobacteria are capable of simultaneously evolving O(2) through oxygenic photosynthesis and fixing nitrogen via nitrogenase. Since nitrogenase is irreversibly inactivated by O(2), accommodation of the two metabolic pathways has led to biochemical and/or structural adaptations that protect the enzyme from O(2). In some species, differentiated cells (heterocysts) are produced within the filaments. PSII is absent in the heterocysts, while PSI activity is maintained. In other, nonheterocystous species, however, a division of labor occurs whereby individual cells within a colony appear to ephemerally fix nitrogen while others evolve oxygen. Using membrane inlet mass spectrometry (MIMS) in conjunction with tracer (18)O(2) and inhibitors of photosynthetic and respiratory electron transport, we examined the light dependence of O(2) consumption in Trichodesmium sp. IMS 101, a nonheterocystous, colonial cyanobacterium, and Anabaena flos-aquae (Lyngb.) Breb. ex Bornet et Flahault, a heterocystous species. Our results indicate that in both species, intracellular O(2) concentrations are maintained at low levels by the light-dependent reduction of oxygen via the Mehler reaction. In N(2)-fixing Trichodesmium colonies, Mehler activity can consume similar to 75% of gross O(2) production, while in Trichodesmium utilizing nitrate, Mehler activity declines and consumes similar to 10% of gross O(2) production. Moreover, evidence for the coupling between N(2) fixation and Mehler activity was observed in purified heterocysts of Anabaena, where light accelerated O(2) consumption by 3-fold. Our results suggest that a major role for PSI in N(2)-fixing cyanobacteria is to effectively act as a photon-catalyzed oxidase, consuming O(2) through pseudocyclic electron transport while simultaneously supplying ATP in both heterocystous and nonheterocystous taxa.