Reactive oxygen species drive vertical migration in diatom microphytobenthic biofilms: A synergy between motility and xanthophyll cycles to cope with oxidative stress
Intertidal microphytobenthic biofilms, dominated by diatoms, experience daily fluctuations in irradiance, which can lead to oxidative stress within the photosynthetic apparatus through the production and accumulation of reactive oxygen species. To maintain photosynthetic efficiency, benthic diatoms have developed photoprotection strategies, including the mobilization of antioxidant xanthophyll cycles and the ability for vertical migration through the sediment. However, the cellular signaling pathways underlying migration remain poorly characterized. The present study investigates the triggering effect of reactive oxygen species on behavioral and photophysiological responses, through the analysis of lipophilic pigments and fluorescence parameters. To this end, two microphytobenthic communities: one allowing vertical migration (with sediment) and one restricting it (without sediment), are exposed to irradiance, cold atmospheric plasma, and hydrogen peroxide stresses. Results highlight a plastic downward migration, under all oxidative stress conditions, suggesting a key role of reactive oxygen species, especially hydrogen peroxide, in triggering and mediating this behavior in microphytobenthos. Moreover, all stresses lead to a decrease in cellular photosynthetic efficiency. Irradiance stress is accompanied by the induction of non-photochemical quenching, resulting from a full activation of the violaxanthin–antheraxanthin–zeaxanthin and diadinoxanthin–diatoxanthin cycles, with a stronger engagement in sediment-lacking communities. In contrast, the two other stresses trigger only a partial xanthophyll mobilization, without inducing effective non-photochemical quenching. By establishing that migration driven by reactive oxygen species represents a rapid and efficient strategy, acting in synergy with xanthophyll for epipelic cell photoprotection, this study provides key insights into the molecular basis of MPB responses to cellular and environmental oxidative stress.