The xanthophyll cycle balances photoprotection and photosynthetic efficiency in the seawater alga Nannochloropsis oceanica

Photosynthetic reactions are continuously modulated to respond to highly dynamic environmental conditions. Balancing photosynthesis and photoprotection involves various mechanisms, which differ across phylogenetic groups. One such mechanism that is widespread in photosynthetic eukaryotes is the xanthophyll cycle, which involves the reversible light-dependent conversion between the carotenoids violaxanthin, antheraxanthin, and zeaxanthin. In this study, we investigated the role of the xanthophyll cycle in Nannochloropsis oceanica, a seawater microalga that possesses peculiarly high xanthophyll levels. To this end, we generated and characterized lines with increased levels of the enzymes involved in the xanthophyll cycle, i.e. violaxanthin de-epoxidase (VDE) and zeaxanthin epoxidase (ZEP). We demonstrated that the level of VDE and ZEP is the main factor controlling the overall reaction rates and dynamics of the xanthophyll cycle. Subsequent differences in the xanthophyll profile affect the activation of photoprotection mechanisms such as nonphotochemical quenching and tolerance to reactive oxygen species. Interestingly, VDE overexpression enhances high light tolerance, whereas increased ZEP levels facilitate faster recovery after light exposure but also heighten photosensitivity under certain conditions. In addition, light exposure strongly downregulates ZEP activity in Nannochloropsis. Taken together, these findings underscore the critical role of the xanthophyll cycle in regulating photosynthesis in Nannochloropsis. This cycle is not simply a mechanism that responds to excess illumination, but one that balances photoprotection and light-use efficiency under different environmental conditions.