Extracellular superoxide production is a widespread photoacclimation strategy in phytoplankton

Phytoplankton control the habitability of Earth. These photosynthetic microorganisms serve as the base of marine food webs, produce approximately half of the planets oxygen, and regulate climate by sequestering carbon dioxide from the atmosphere. As global changes accelerate through the Anthropocene, phytoplankton communities face multiple stressors, including warming, shifting patterns in ocean circulation and structure, and associated perturbations in levels of light exposure. The health and functioning of the oceans depends on phytoplankton community responses to these stressors; however, the physiological processes involved in light stress are not fully understood. Here, we surveyed sixteen 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 regulated extracellular superoxide production as a function of light exposure, which was modeled with a modified photosynthesis-irradiance (PE) curve. Furthermore, the flavoenzyme inhibitor DPI quenched extracellular superoxide production and lead to declines in viability and photosynthetic health in thirteen out of sixteen 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.