Nutrient deficiency stimulates the production of superoxide in the noxious red-tide-forming raphidophyte Chattonella antiqua

Abstract

The raphidophyte Chattonella antiqua is a single-celled alga that forms ‘red tides’ in coastal areas. C. antiqua produces superoxide anions (O2−), the excessive production of which has been associated with fish mortality. It is suggested that putative NADPH oxidase in the outer membrane oxidizes intracellular NADPH to produce O2− and secrete it externally. Earlier studies revealed that photosynthetic electron transport, a major producer of NADPH in photosynthetic organisms, is involved in the production of O2− in C. antiqua but the details of the O2− production mechanism have yet to be elucidated. Since nutrient deficiency adversely affects the formation of blooms of C. antiqua, in this study, we examined the effects of nutrient deficiency on O2− production in C. antiqua. When cells were grown under nitrogen (N)- or phosphorus (P)-deficient conditions, the production of O2− was stimulated. In particular, the extracellular levels of O2− under N- or P-deficient conditions were high during the dark period when photosynthetic activities in terms of actual quantum efficiency and photochemical quenching were low. The extracellular levels of O2− under the nutrient-deficient conditions were unaffected by the presence of 3-(3,4-dichlorophenyl)-1,1‑dimethylurea (DCMU), an inhibitor of photosynthetic electron transport, but decreased when the nutrients were present. Furthermore, the intracellular ratio of NADPH to NADP+ under N- or P-deficient conditions was higher than that under nutrient-replete conditions. These observations suggest that another metabolic pathway, independent of photosynthesis, provides NADPH for the production of O2− under nutrient deficiency.