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Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence [Biophysics and Computational Biology]
Proceedings of the National Academy of Sciences of the United States of America ( IF 11.1 ) Pub Date : 2021-02-02 , DOI: 10.1073/pnas.2005944118
Francesco Carrara 1 , Anupam Sengupta 1, 2 , Lars Behrendt 1, 3 , Assaf Vardi 4 , Roman Stocker 1
Affiliation  

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.



中文翻译:

氧化应激反应的双稳态决定了浮游植物在湍流中的迁移行为[生物物理学和计算生物学]

湍流是浮游植物生理的重要决定因素,通常会导致细胞应激和损伤。湍流通过运输细胞和触发迁徙行为的开关来影响浮游植物的迁移,从而垂直迁移的细胞在暴露于湍流线索后可以主动反转其迁移方向。但是,目前缺少单细胞生理学和湍流中浮游植物的垂直迁移之间的机械联系。在这里,通过将生理和行为实验与应力积累和消散的数学模型相结合,我们证明了在海洋斜纹藻类杂种赤足鱼中迁移方向转换的机制。是由湍流线索生成的活性氧(ROS)信号的整合。在短短数十秒的时间范围内,与向上迁移的亚种群相比,新兴的向下迁移的亚种群表现出ROS的两倍增长,这是胁迫的指标,光合效率降低了15%,多代生长速率降低了35%。通过观察到细胞暴露于外源性应激源(H 2 O 2),证实了由于双稳态氧化应激反应而导致的行为分裂的起源。(例如UV-A辐射或高辐照度)代替湍流,引起相当的ROS积累,并等效地分成两个亚群。通过在一方面的游泳和生理学的单细胞机制与另一方面出现的人口规模迁移反应以及对健康的影响之间建立机制联系,我们发现了ROS介导的预警反应有助于我们对浮游植物的理解。未来海洋条件下的群落组成。

更新日期:2021-01-26
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