Production of extracellular superoxide contributes to photosynthesis via elimination of reducing power and regeneration of NADP+ in the red-tide-forming raphidophyte Chattonella marina complex

The raphidophyte Chattonella marina complex (hereafter Chattonella) consists of noxious red-tide-forming algae that are damaging to fish farms. Chattonella produces and secretes large amounts of the superoxide anion (•O₂^-), and the production of extracellular •O₂^- has been associated with fish mortality. We reported previously that photosynthetic electron transport is correlated with the production of •O₂^- in the genus Chattonella. However, the physiological roles of the production of extracellular •O₂^- remain to be clarified. In the present study, we examined the effects of the production of extracellular •O₂^- on photosynthesis and cell proliferation in two strains of Chattonella, namely, Ago03, a highly toxic strain that produces large amounts of •O₂^- externally, and Ago04, a low-toxicity strain that produces very small amounts of •O₂^-. Both the growth rate and the net photosynthetic activity of Ago04 were higher than those of Ago03. In Ago04, levels of Rubisco and 3-phosphoglycerate, the product of the reaction catalyzed by Rubisco, were 4-fold higher than those in Ago03, suggesting the higher photosynthetic activity of Ago04. In the presence of glycolaldehyde, a specific inhibitor of the Calvin-Benson cycle, the levels of NADP⁺ and the photosynthetic parameter qP declined under strong light in Ago04. By contrast, levels of NADP⁺ and qP in Ago03 changed less significantly than those in Ago04. Given that •O₂^- is produced by a putative NADPH oxidase that converts O₂ to •O₂^- in Chattonella, it seems likely that the production of •O₂^- might play a role not only in the elimination of excess reducing power of NADPH from the cell, via •O₂^-, but also in the regeneration of NADP⁺, as a result of the action of NADPH oxidase, which oxidizes NADPH, to maintain photosynthetic electron transport.