Nonphotochemical quenching and beyond: multi-layered photoprotection shapes light-stress tolerance across seasonal niches in Arctic diatoms

Throughout their species seasonal succession, diatoms of the Arctic Ocean experience a radical habitat transformation, from surviving the dimly lit winter within sea-ice or in the water column, to rapid growth under increasing irradiances, forming massive spring blooms beneath melting ice and later in open waters. Therefore, their evolutionary path has been moulded by the opposing challenges of maximizing light capture part of the year while maintaining highly efficient photoprotection capacities to limit photodamage upon bursts of supra-optimal illumination. Two main photoprotection mechanisms exist in diatoms i) nonphotochemical quenching (NPQ) supported primarily by the xanthophyll cycle (XC) and stress-related Lhcx antenna proteins and, ii) a rapid repair cycle of photosystem (PS) II core protein, PsbA, upon photodamage. Previous studies suggest that freezing temperatures slow protein turnover and favour photoprotection strategies that rely primarily upon XC-NPQ in polar taxa. We aim to revisit this hypothesis by dissecting the high-light response of five Arctic diatom species that dominate contrasting ecological niches: sea-ice, marginal ice-zone and open waters. We exposed each species to a high-light stress and subsequent recovery period under low light, with and without, inhibitors of XC-NPQ (dithiothreitol) or of plastid protein translation (lincomycin), blocking de novo replacement of PsbA. We confirmed the crucial role of XC-NPQ in protecting PSII but also report unexpected observations that challenge our current understanding of psychrophile species response to light stress. First, the impact of lincomycin on PSII photoinhibition was stronger than that of DTT, despite PsbA turnover being undetectable by immunoblots in most cases. Second, while our data support planktonic species showing better tolerance to high light than sympagic species, we found unsuspected diversity in photoprotection strategies. We hypothesize that these differences support a gradient from conservative strategies, possibly optimized for survival in the extreme sea-ice habitat of sympagic species, to productivity-oriented strategies in open water planktonic species dominating during the bloom period. In the transforming, brighter, Arctic Ocean, the adaptedness of this community-wide strategy scheme could be undermined, shaking up the historical dominance of certain diatom taxa.