Cyanobacterial Lactate Oxidases Serve as Essential Partners in N2 Fixation and Evolved into Photorespiratory Glycolate Oxidases in Plants (original) (raw)
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All colonial diazotrophic cyanobacteria are capable of simultaneously evolving O2 through oxygenic photosynthesis and fixing nitrogen via nitrogenase. Since nitrogenase is irreversibly inactivated by O2, accommodation of the two metabolic pathways has led to biochemical and ⁄ or structural adaptations that protect the enzyme from O2. 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 18O2 and inhibitors of photosynthetic and respiratory electron transport, we examined the light dependence of O2 consumption in Trichodesmium sp. IMS 101, a nonheterocystous, colonial cyanobacterium, and Anabaena flos-aquae (Lyngb.) Bre´b. ex Bornet et Flahault, a heterocystous species. Our results indicate that in both species, intracellular O2 concentrations are maintained at low levels by the light-dependent reduction of oxygen via the Mehler reaction. In N2-fixing Trichodesmium colonies, Mehler activity can consume 75% of gross O2 production, while in Trichodesmium utilizing nitrate, Mehler activity declines and consumes 10% of gross O2 production. Moreover, evidence for the coupling between N2 fixation and Mehler activity was observed in purified heterocysts of Anabaena, where light accelerated O2 consumption by 3-fold. Our results suggest that a major role for PSI in N2-fixing cyanobacteria is to effectively act as a photoncatalyzed oxidase, consuming O2 through pseudocyclic electron transport while simultaneously supplying ATP in both heterocystous and nonheterocystous taxa.
Cyanobacteria have played a profound role in shaping the biosphere, most notably through the Great Oxygenation Event (GOE) with the advent of photosynthesis1. Cyanobacteria also contribute to global primary production through biological nitrogen fixation (BNF) using nitrogenase2,3, an oxygen-labile enzyme complex that evolutionarily predates the GOE4. Current literature reports nitrogenase activity in unicellular cyanobacteria is protected from oxygen through diurnal separation of photosynthesis and BNF5. However, historic conditions of continuous-light and warm temperature at polar latitudes during the Triassic and Cretaceous may have created a selective advantage amongst unicellular cyanobacteria for non-temporal mechanisms of maintaining nitrogenase activity in the presence of oxygen. Here we report constitutive nitrogenase activity concurrent with a net-gain of oxygen through photosynthesis in a continuous-light adapted culture of the unicellular cyanobacteria, Cyanothece sp. AT...