Reactive oxygen species drive 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 the mobilization of antioxidant xanthophyll cycle and the ability for vertical migration through the sediment. However, the cellular signaling pathways underlying migration remain 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 and driving this microphytobenthic behavior. Moreover, a difference was observed between the pathways involved in vertical migration and those underlying the photophysiological response. Hydrogen peroxide and cold atmospheric plasma stresses highlighted the necessity of substantial microphytobenthic migration, whereas irradiance induced a specific and controlled response involving engagement of the xanthophyll cycles, acting in synergy with the migration strategy by showing stronger activation when migration was impaired. By establishing that the rapid and efficient migration strategy, acting in synergy with xanthophyll cycles in epipelic cells, is induced by reactive oxygen species, this study provides key insights into the molecular basis of microphytobenthic responses to cellular and environmental oxidative stress. GRAPHICAL ABSTRACT