期刊
出版社
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2005944118
关键词
ROS; motility; photophysiology; harmful-algal-bloom; intermittency
资金
- Gordon and Betty Moore Foundation Marine Microbial Initiative Investigator Award [GBMF3783]
- Gordon and Betty Moore Symbiosis in Aquatic Systems Investigator Award [GBMF9197]
- Simons Foundation as part of the Principles of Microbial Ecosystems Collaborative (PriME) [542395]
- Swiss National Science Foundation [315230_176189]
- Israeli Science Foundation [712233]
- Science for life Laboratory
- Independent Research Fund Denmark [DFF-1323-00747/DFF-1325-00069]
- Swedish Research Council [2019-04401]
- Human Frontier Science Program Cross Disciplinary Fellowship [LT000993/2014-C]
- ATTRACT Investigator Grant of the Luxembourg National Research Fund [A17/MS/11572821/MBRACE]
- Swedish Research Council [2019-04401] Funding Source: Swedish Research Council
- Vinnova [2019-04401] Funding Source: Vinnova
- Swiss National Science Foundation (SNF) [315230_176189] Funding Source: Swiss National Science Foundation (SNF)
This study reveals that the switch in migration direction of the marine raphidophyte Heterosigma akashiwo under turbulence is due to the integration of reactive oxygen species signaling. Exposure of cells to exogenous stressors can also lead to ROS accumulation and the split into two subpopulations. This mechanistic link between single-cell mechanics and population-scale migratory response contributes to the understanding of phytoplankton community composition in future ocean conditions.
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.
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