Pennate diatoms make non-photochemical quenching as simple as possible but not simpler

Studies of marine microalgal photosynthesis are heavily moulded on legacy research from organisms like Arabidopsis and Chlamydomonas, despite the differences between primary and secondary endosymbionts. Non-photochemical quenching (NPQ) protects photosystem II from excessive light and, in pennate diatoms, requires the xanthophyll pigment diatoxanthin and Lhcx proteins. Although NPQ’s relationship with diatoxanthin is straightforward, the role of Lhcx proteins has been unclear and at the core of several conflicting NPQ models, often unnecessarily borrowing the complexity of models from green organisms. We use 14 Phaeodactylum tricornutum strains, including 13 transgenic lines with variable Lhcx1 expression levels, grow them under two non-stressful light conditions, and modulate diatoxanthin levels through short light stress. The resulting Lhcx1-diatoxanthin matrices are used to demonstrate that NPQ is proportional to the product of the Lhcx1 concentration and the proportion of diatoxanthin in the xanthophyll pool. This indicates that the interaction between diatoxanthin and Lhcx1 creates a homogeneous Stern-Volmer quencher responsible for NPQ. Additionally, we demonstrate that the photosynthetic unit in pennate diatoms follows a “lake” model, with discrepancies in the NPQ-photochemistry relationship arising from unconsidered assumptions, one possibility being cellular heterogeneity. This underscores pennate diatoms as natural reductionist system for studying marine photosynthesis.