Synergistic effects of temperature and light on photoprotection in the model diatom Phaeodactylum tricornutum

Diatoms dominate phytoplankton communities in turbulent waters, where light fluctuations can be frequent and intense. Due to this complex environment, these heterokont microalgae display remarkable photoprotection strategies, including a fast Non-Photochemical Quenching (NPQ). However, in nature, several abiotic parameters (such as temperature) can influence the response of photosynthetic organisms to light stress in a synergistic or antagonistic manner. Yet, the combined effects of light and these other drivers on the photosynthetic and photoprotective capacity of diatoms are still poorly understood. In this work, we investigated the impact of short-term temperature and light stress on the model diatom Phaeodactylum tricornutum, combining NPQ induction-recovery assays or light curves with a broad gradient of superimposed temperature treatments (5 to 35°C). We employed mutant lines deficient in NPQ generation (vde KO) or recovery (zep3 KO) and wild type. We found that temperature and light have a synergistic effect: lower temperatures limited both the photosynthetic capacity and NPQ, while the general photophysiological performance was enhanced with warming, up to a heat-stress limit (above 30°C). We discuss the temperature effects on NPQ induction and recovery and propose that these are independent from the energy requirements of the cells and result from altered xanthophyll cycle dynamics. Namely, we found that de-epoxidation activity strongly increases with temperature, outweighing epoxidation and resulting in a positive increase of NPQ with temperature. Finally, we propose that in a short-term time frame, temperature and light have a synergistic and not antagonistic effect, with a positive relationship between increasing temperature and NPQ.