Structural and quantum chemical basis for OCP-mediated quenching of phycobilisomes

Sauer, Paul V.; Cupellini, Lorenzo; Sutter, Markus; Bondanza, Mattia; Domínguez Martin, María Agustina; Kirst, Henning; Bína, David; Koh, Adrian Fujiet; Kotecha, Abhay; Greber, Basil J.; Nogales, Eva; Polívka, Tomáš; Mennucci, Benedetta; Kerfeld, Cheryl A.

doi:10.1126/sciadv.adk7535

Title: Structural and quantum chemical basis for OCP-mediated quenching of phycobilisomes

Journal Article · 04 April 2024 · Science Advances

DOI: https://doi.org/10.1126/sciadv.adk7535 · OSTI ID:2448504

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Univ. of California, Berkeley, CA (United States)
Universita di Pisa (Italy)
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Universidad de Córdoba (Spain)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba (Spain)
University of South Bohemia, Ceske Budejovice (Czech Republic); Czech Academy of Sciences (CAS), Ceske Budejovice (Czech Republic)
Thermo Fisher Scientific, Eindhoven (Netherlands)
Institute of Cancer Research, London (United Kingdom)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
University of South Bohemia, Ceske Budejovice (Czech Republic)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0020606

OSTI ID:: 2448504

Journal Information:: Science Advances, Journal Name: Science Advances Journal Issue: 14 Vol. 10; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

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