Lhcx proteins provide photoprotection via thermal dissipation of absorbed light in the diatom Phaeodactylum tricornutum

Jochen M Buck,Marc Halder,Angela Falciatore,Manuel Serif,Paul G Falkowski,Jonathan Sherman,Carolina Río Bártulos,Johann Lavaud,Maxim Y Gorbunov,Bernard Lepetit,Jan Henkel,Peter G Kroth

doi:10.1038/s41467-019-12043-6

Abstract

Diatoms possess an impressive capacity for rapidly inducible thermal dissipation of excess absorbed energy (qE), provided by the xanthophyll diatoxanthin and Lhcx proteins. By knocking out the Lhcx1 and Lhcx2 genes individually in Phaeodactylum tricornutum strain 4 and complementing the knockout lines with different Lhcx proteins, multiple mutants with varying qE capacities are obtained, ranging from zero to high values. We demonstrate that qE is entirely dependent on the concerted action of diatoxanthin and Lhcx proteins, with Lhcx1, Lhcx2 and Lhcx3 having similar functions. Moreover, we establish a clear link between Lhcx1/2/3 mediated inducible thermal energy dissipation and a reduction in the functional absorption cross-section of photosystem II. This regulation of the functional absorption cross-section can be tuned by altered Lhcx protein expression in response to environmental conditions. Our results provide a holistic understanding of the rapidly inducible thermal energy dissipation process and its mechanistic implications in diatoms.

Highlights

Diatoms possess an impressive capacity for rapidly inducible thermal dissipation of excess absorbed energy, provided by the xanthophyll diatoxanthin and Lhcx proteins
The very low Non-Photochemical Quenching (NPQ) values obtained after 3 min of supra-optimal light exposure in the x1KO lines even increased during the following dark phase, indicating it is not of qE origin
To prove that the observed phenotype is related to the knockout of Lhcx[1], we complemented the independent x1KO_1a and x1KO_2 lines with an Lhcx[1] gene that was modified at the TALEN-binding sites by synonymous codon usage, in order to prevent a recutting by the TALEN system

Summary

Introduction

Diatoms possess an impressive capacity for rapidly inducible thermal dissipation of excess absorbed energy (qE), provided by the xanthophyll diatoxanthin and Lhcx proteins. We establish a clear link between Lhcx1/2/3 mediated inducible thermal energy dissipation and a reduction in the functional absorption cross-section of photosystem II. In oxygenic photosynthetic organisms, photon capture can be regulated by adjusting the cross-section of photosystem II on time scales of minutes This phenomenon leads to changes in the balance between excitons directed to reaction centers and those that are dissipated as heat. There are a number of photoprotective mechanisms that thermally dissipate excess absorbed energy as heat; collectively these are called Non-Photochemical Quenching (NPQ) This phenomenon is present in all photosynthetic eukaryotes and in many cyanobacteria[1,2,3], and is characterized by a downregulation of chlorophyll fluorescence at high irradiance. The correlation between the onset of qE and the reduction of σPSII has recently been challenged[11]

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