Reactive oxygen species drive vertical migration in diatom microphytobenthic biofilms: A synergy between motility and xanthophyll cycles to cope with oxidative stress

Diatom-dominated 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 investigatesd 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 anotherone without sediment -thus without movement- restricting it (without sediment), weare exposed to irradiance, cold atmospheric plasma, and hydrogen peroxide stresses. Results highlighted a plastic downward migration response, 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 wais 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 triggered only a partial activation of the xanthophyll cyclemobilization, 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 the xanthophyll cycle for epipelic cell photoprotection, this study provides key insights into the molecular basis of MPB responses to cellular and environmental oxidative stress.