Extracellular superoxide production is a widespread photoacclimation strategy in phytoplankton

Phytoplankton help control the habitability of Earth by serving as the base of marine food webs, producing approximately half of the planet's oxygen, and sequestering carbon dioxide from the atmosphere. As global changes accelerate through the Anthropocene, phytoplankton communities face multiple stressors, such as shifting patterns in ocean circulation, and associated changes in light exposure. The health of the oceans depends on phytoplankton responses to these stressors; however, the physiological processes involved in light stress are not fully understood. Here, we surveyed 16 representative phytoplankton and show that most produce extracellular superoxide, an otherwise damaging reactive oxygen species, as a widespread strategy to acclimate to light stress. Indeed, all species adjusted extracellular superoxide production as a function of light exposure, which was modeled with a modified photosynthesis-irradiance (PI) curve. Furthermore, the flavoenzyme inhibitor diphenyl iodonium (DPI) quenched extracellular superoxide production and led to declines in viability and photosynthetic health in 13 out of 16 species. The negative effect of DPI on photosynthetic health was stronger with increasing light, consistent with inhibition of a photoprotective process. Taken together, these results support the hypothesis that phytoplankton mitigate light stress through enzyme-mediated production of extracellular superoxide. These results imply that daytime rates of biological superoxide production in the marine environment are substantially underestimated by dark measurements. Furthermore, phytoplankton photoacclimation may alter superoxide production rates in future oceans impacted by changes in water column structure and light exposure.