The Xanthophyll Cycle balances Photoprotection and Efficiency in the seawater alga Nannochloropsis oceanica

Abstract

Photosynthetic reactions require continuous modulation to respond to highly dynamic environmental conditions. Regulation of photosynthesis involves various mechanisms, which differ across phylogenetic groups. One such mechanism, found 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 impact of the xanthophyll cycle in Nannochloropsis oceanica, a seawater microalga member of Eustigmatophyta that features a peculiarly high content of xanthophylls. 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) and demonstrated that their content is a main factor in controlling the overall reaction rates and the dynamics of the xanthophyll cycle. Subsequent differences in the xanthophyll profile affect the activation of photoprotection mechanisms such as non-photochemical quenching and tolerance to reactive oxygen species. Interestingly, overexpression of VDE expands the limits of high light tolerance, whereas the increased content of ZEP facilitates faster recovery after exposure to light but also heightened photosensitivity under some conditions. These findings underscore the critical role of the xanthophyll cycle in the regulation of photosynthesis in Nannochloropsis, where it is not simply a mechanism to respond to excess illumination, but plays a central role in modulating photosynthesis, fulfilling the complex task of balancing photoprotection and light-use efficiency under different environmental conditions.