Cyanobacteria use large antenna complexes called phycobilisomes (PBSs) for light harvesting. However, intense light triggers non-photochemical quenching, where the orange carotenoid protein (OCP) binds to PBS, dissipating excess energy as heat. The mechanism of efficiently transferring energy from phycocyanobilins in PBS to canthaxanthin in OCP remains insufficiently understood. Using cryo-electron microscopy, we unveiled the OCP-PBS complex structure at 1.6- to 2.1-angstrom resolution, showcasing its inherent flexibility. Using multiscale quantum chemistry, we disclosed the quenching mechanism. Identifying key protein residues, we clarified how canthaxanthin's transition dipole moment in its lowest-energy dark state becomes large enough for efficient energy transfer from phycocyanobilins. Our energy transfer model offers a detailed understanding of the atomic determinants of light harvesting regulation and antenna architecture in cyanobacteria.

Biology Centre of the Czech Academy of Sciences Ceske Budejovice Czech Republic

California Institute for Quantitative Biosciences University of California Berkeley CA 94720 USA

Department of Biochemistry and Molecular Biology Michigan State University East Lansing MI 48824 USA

Department of Molecular and Cellular Biology University of California Berkeley CA 94720 USA

Dipartimento di Chimica e Chimica Industriale Università di Pisa Via G Moruzzi 13 1 56124 Pisa Italy

Division of Structural Biology The Institute of Cancer Research London SW7 3RP UK

Environmental Genomics and Systems Biology Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA

Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic

Howard Hughes Medical Institute University of California Berkeley CA 94720 USA

Molecular Biophysics and Integrated Bioimaging Division Lawrence Berkeley National Laboratory Berkeley CA 94720 USA

MSU DOE Plant Research Laboratory Michigan State University East Lansing MI 48824 USA

Thermo Fisher Scientific Eindhoven Netherlands

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