Thylakoid plasticity primes photoprotection in diatoms

Abstract

For many millions of years, diatoms have been major primary producers in marine ecosystems, supporting food webs and contributing to carbon sequestration through the export of photosynthetically fixed carbon to the deep ocean, mitigating atmospheric carbon dioxide levels and global climate. A key factor in their ecological success is their ability to rapidly adapt to fluctuating light, balancing efficient light harvesting under dim conditions with energy dissipation under excess light. However, the mechanisms behind this regulation have not been fully elucidated. This study shows that several processes contribute to dissipating excess excitation energy in diatoms exposed to light stress: (i) the detachment of the oxygen-evolving complex proteins from the PSII core, leading to energy dissipation via charge recombination, (ii) Non-Photochemical Quenching (NPQ) in the antenna, i.e., thermal dissipation of excited states and (iii) excitation energy transfer from PSII to PSI via energy spillover. The latter process is observed in parallel with high light-induced topological changes of the thylakoids that may favor transient interactions between the photosystems. Along with the accumulation of light-stress-protecting carotenoids on longer time-scales, this ensemble of photoprotective mechanisms provides a dynamic and flexible response to the light challenges expected in coastal marine habitats.