[en] 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 actively 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 twofold increase in 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 as a result of 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 the single-cell mechanics of swimming and physiology on the one side and the emergent population-scale migratory response and impact on fitness on the other, the ROS-mediated early warning response we discovered contributes to our understanding of phytoplankton community composition in future ocean conditions.
Physical, chemical, mathematical & earth Sciences: Multidisciplinary, general & others
Author, co-author :
Carrara, Francesco ✱; ETH Zurich, Switzerland
Sengupta, Anupam ✱; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Physics and Materials Science (DPHYMS)
Behrendt, Lars; Uppsala University, Sweden
Vardi, Assaf; Weizmann Institute of Science, Israel
Stocker, Roman; ETH Zurich, Switzerland
✱ These authors have contributed equally to this work.
External co-authors :
Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence
Publication date :
02 February 2021
Journal title :
Proceedings of the National Academy of Sciences of the United States of America
National Academy of Sciences, Washington DC, United States - District of Columbia