TY - JOUR
T1 - Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence
AU - Carrara, Francesco
AU - Sengupta, Anupam
AU - Behrendt, Lars
AU - Vardi, Assaf
AU - Stocker, Roman
N1 - We thank G. Boffetta and M. Cencini for sharing the direct numerical simulations data and Russell Naisbit for help with the editing of this manuscript. This work was supported by Gordon and Betty Moore Foundation Marine Microbial Initiative Investigator Award GBMF3783 (to R.S.), Gordon and Betty Moore Symbiosis in Aquatic Systems Investigator Award GBMF9197 (to R.S.; https://doi.org/10.37807/GBMF9197), and Simons Foundation Grant 542395 (to R.S.) as part of the Principles of Microbial Ecosystems Collaborative (PriME), Swiss National Science Foundation Grant 315230_176189 (to R.S.), the Israeli Science Foundation grant 712233 (to A.V.), funding from the Science for life Laboratory (to L.B.), the Independent Research Fund Denmark (DFF-1323-00747/DFF-1325-00069) (to L.B.), the Swedish Research Council (2019-04401) (to L.B.), the Human Frontier Science Program Cross Disciplinary Fellowship LT000993/2014-C (to A.S.), and the ATTRACT Investigator Grant A17/MS/11572821/MBRACE of the Luxembourg National Research Fund (to A.S.). Author contributions - F.C., A.S., L.B., A.V., and R.S. designed research; F.C., A.S., and L.B. performed research; F.C., A.S., and L.B. analyzed data; and F.C., A.S., L.B., A.V., and R.S. wrote the paper.
PY - 2021/2/2
Y1 - 2021/2/2
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85100007451&partnerID=8YFLogxK
U2 - https://doi.org/10.1073/pnas.2005944118
DO - https://doi.org/10.1073/pnas.2005944118
M3 - مقالة
C2 - 33495340
SN - 0027-8424
VL - 118
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 5
M1 - 2005944118
ER -