Photosynthetic organisms employ light-harvesting complexes (LHCs) to optimize energy capture under variable light conditions. The freshwater eustigmatophyte Trachydiscus minutus accumulates a red-shifted violaxanthin-chlorophyll protein (rVCP) that contributes to far-red light harvesting using only chlorophyll (Chl) a molecules, without chemical modification or substitution of pigments. Based on high-resolution cryo-EM and multiscale quantum chemical calculations, we uncovered a heterodimer-based tetrameric architecture, representing a unique oligomerization mode among LHCs. Within each heterodimer, Chls a are distinctively arranged adjacent to the terminal emitter, forming an unprecedentedly extended chlorophyll cluster. Quantum chemical calculations reveal three strong exciton-coupled pigment domains, two of which reside in the large cluster and solely account for the intense far-red absorption near 700 nm without contributions from charge-transfer states. Our structural and quantum chemical characterizations of far-red light harvesting reveal a molecular mechanism of red spectral tuning that relies on protein-controlled excitonic coupling of identical Chl a pigments, as demonstrated here in this eustigmatophyte, highlighting diverse adaptations for harvesting spectrally shifted, low-energy light.

Centre Algatech Institute of Microbiology Czech Academy of Sciences Novohradská 237 Třeboň 379 01 Czech Republic

Czech Academy of Sciences Biology Centre Institute of Plant Molecular Biology Braniš;ovská 31 České Budějovice 370 05 Czech Republic

Dipartimento di Chimica e Chimica Industriale University of Pisa Via G Moruzzi 13 Pisa 56124 Italy

Graduate School of Frontier Biosciences The University of Osaka Yamadaoka Suita Osaka 565 0871 Japan

Graduate School of Science Osaka City University Sumiyoshi Osaka 558 8585 Japan

Graduate School of Science Osaka Metropolitan University Sumiyoshi Osaka 558 8585 Japan

Institute for Open and Transdisciplinary Research Initiatives The University of Osaka Yamadaoka Suita Osaka 565 0871 Japan

Institute for Protein Research The University of Osaka Suita Osaka 565 0871 Japan

JEOL YOKOGUSHI Research Alliance Laboratories The University of Osaka Yamadaoka Suita Osaka 565 0871 Japan

Research Center for Artificial Photosynthesis Osaka Metropolitan University Sumiyoshi Osaka 558 8585 Japan

University of South Bohemia in České Budějovice Faculty of Science Braniš;ovská 1760 České Budějovice 370 05 Czech Republic

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