Dynamic Regulation of Extracellular Superoxide Production by the Coccolithophore Emiliania huxleyi (CCMP 374)

In marine waters, ubiquitous reactive oxygen species (ROS) drive biogeochemical cycling of metals and carbon. Marine phytoplankton produce the ROS superoxide (O(2)(−)) extracellularly and can be a dominant source of O(2)(−) in natural aquatic systems. However, the cellular regulation, biological functioning, and broader ecological impacts of extracellular O(2)(−) production by marine phytoplankton remain mysterious. Here, we explored the regulation and potential roles of extracellular O(2)(−) production by a noncalcifying strain of the cosmopolitan coccolithophorid Emiliania huxleyi, a key species of marine phytoplankton that has not been examined for extracellular O(2)(−) production previously. Cell-normalized extracellular O(2)(−) production was the highest under presumably low-stress conditions during active proliferation and inversely related to cell density during exponential growth phase. Removal of extracellular O(2)(−) through addition of the O(2)(−) scavenger superoxide dismutase (SOD), however, increased growth rates, growth yields, cell biovolume, and photosynthetic efficiency (F(v)/F(m)) indicating an overall physiological improvement. Thus, the presence of extracellular O(2)(−) does not directly stimulate E. huxleyi proliferation, as previously suggested for other phytoplankton, bacteria, fungi, and protists. Extracellular O(2)(−) production decreased in the dark, suggesting a connection with photosynthetic processes. Taken together, the tight regulation of this stress independent production of extracellular O(2)(−) by E. huxleyi suggests that it could be involved in fundamental photophysiological processes.