Reactive oxygen species trigger downward vertical migration in diatom microphytobenthic biofilms as a strategy to cope with oxidative stress

Diatom-dominated intertidal microphytobenthic biofilms 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 protective strategies, including mobilization of the antioxidant xanthophyll cycle and the ability to migrate vertically through sediments. However, mechanistic understanding of signaling pathways underlying migration remains poorly characterized. This study investigated 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 with sediment allowing vertical migration and another without sediment restricting it, were exposed to irradiance, cold atmospheric plasma, and hydrogen peroxide stresses. Results showed a consistent downward migration response under all oxidative stresses, highlighting the key role of reactive oxygen species, especially hydrogen peroxide, in triggering this microphytobenthic behavior. Moreover, a difference was observed between the pathways involved in vertical migration and those underlying photoprotective responses. Hydrogen peroxide and cold atmospheric plasma stresses highlighted the necessity for substantial microphytobenthic migration, whereas irradiance induced a specific and controlled response involving engagement of the xanthophyll cycle, acting in synergy with the migration strategy by showing stronger activation when migration was impaired. By establishing that a rapid and efficient migration could be induced by reactive oxygen species and could act in synergy with the xanthophyll cycle in epipelic cells, this study provides key insights into the molecular basis of microphytobenthic responses to cellular and environmental oxidative stresses.