Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence

Turbulence is an important determinant of phytoplankton physiology, often leading to cell stress and damage. Turbulence affects phytoplankton migration, both by transporting cells and by triggering switches in migratory behavior, whereby vertically migrating cells can invert their direction of migration upon exposure to turbulent cues. However, a mechanistic link between single-cell physiology and vertical migration of phytoplankton in turbulence is currently missing. Here, by combining physiological and behavioral experiments with a mathematical model of stress accumulation and dissipation, we show that the mechanism responsible for the switch in the direction of migration in the marine raphidophyte Heterosigma akashiwo is the integration of reactive oxygen species (ROS) signaling generated by turbulent cues. Within timescales as short as tens of seconds, the emergent downward-migrating subpopulation exhibited a two-fold increase of ROS, an indicator of stress, 15% lower photosynthetic efficiency, and 35% lower growth rate over multiple generations compared to the upward-migrating subpopulation. The origin of the behavioral split in a bistable oxidative stress response is corroborated by the observation that exposure of cells to exogenous stressors (H2O2, UV-A radiation or high irradiance), in lieu of turbulence, caused comparable ROS accumulation and an equivalent split into the two subpopulations. By providing a mechanistic link between single-cell physiology, population-scale migration and fitness, these results contribute to our understanding of phytoplankton community composition in future ocean conditions. Significance StatementTurbulence has long been known to drive phytoplankton fitness and species succession: motile species dominate in calmer environments and non-motile species in turbulent conditions. Yet, a mechanistic understanding of the effect of turbulence on phytoplankton migratory behavior and physiology is lacking. By combining a method to generate turbulent cues, quantification of stress accumulation and physiology, and a mathematical model of stress dynamics, we show that motile phytoplankton use their mechanical stability to sense the intensity of turbulent cues and integrate these cues in time via stress signaling to trigger switches in migratory behavior. The stress-mediated warning strategy we discovered provides a paradigm for how phytoplankton cope with turbulence, thereby potentially governing which species will be successful in a changing ocean.