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

Francesco Carrara; Anupam Sengupta; Lars Behrendt; Assaf Vardi; Roman Stocker

doi:10.1073/pnas.2005944118

Edited by Edward F. DeLong, University of Hawaii at Manoa, Honolulu, HI, and approved December 11, 2020 (received for review March 30, 2020)

Significance

Turbulence 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.

Abstract

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.

Footnotes

↵¹F.C. and A.S. contributed equally to this work.
↵²To whom correspondence may be addressed. Email: anupam.sengupta{at}uni.lu or romanstocker{at}ethz.ch.

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.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2005944118/-/DCSupplemental.