The Orange Carotenoid Protein Triggers Cyanobacterial Photoprotection by Quenching Bilins Via a Structural Switch of Its Carotenoid

Overview

Journal J Am Chem Soc

Publisher American Chemical Society

Specialty Chemistry

Date 2024 Jul 26

PMID 39058977

Authors

Nicoletta Liguori

Ivo H M van Stokkum

Fernando Muzzopappa

John T M Kennis

Diana Kirilovsky

Roberta Croce

Affiliations

Soon will be listed here.

Abstract

Cyanobacteria were the first microorganisms that released oxygen into the atmosphere billions of years ago. To do it safely under intense sunlight, they developed strategies that prevent photooxidation in the photosynthetic membrane, by regulating the light-harvesting activity of their antenna complexes-the phycobilisomes-via the orange-carotenoid protein (OCP). This water-soluble protein interacts with the phycobilisomes and triggers nonphotochemical quenching (NPQ), a mechanism that safely dissipates overexcitation in the membrane. To date, the mechanism of action of OCP in performing NPQ is unknown. In this work, we performed ultrafast spectroscopy on a minimal NPQ system composed of the active domain of OCP bound to the phycobilisome core. The use of this system allowed us to disentangle the signal of the carotenoid from that of the bilins. Our results demonstrate that the binding to the phycobilisomes modifies the structure of the ketocarotenoid associated with OCP. We show that this molecular switch activates NPQ, by enabling excitation-energy transfer from the antenna pigments to the ketocarotenoid.

Citing Articles

Two-Photon-Driven Photoprotection Mechanism in Echinenone-Functionalized Orange Carotenoid Protein.

Nizinski S, Hartmann E, Shoeman R, Tarnawski M, Wilson A, Reinstein J J Am Chem Soc. 2025; 147(5):4100-4110.

PMID: 39836707 PMC: 11803624. DOI: 10.1021/jacs.4c13341.

References

Dominguez-Martin M, Sauer P, Kirst H, Sutter M, Bina D, Greber B . Structures of a phycobilisome in light-harvesting and photoprotected states. Nature. 2022; 609(7928):835-845. DOI: 10.1038/s41586-022-05156-4. View

Liguori N, Xu P, van Stokkum I, van Oort B, Lu Y, Karcher D . Different carotenoid conformations have distinct functions in light-harvesting regulation in plants. Nat Commun. 2017; 8(1):1994. PMC: 5722816. DOI: 10.1038/s41467-017-02239-z. View

Jallet D, Thurotte A, Leverenz R, Perreau F, Kerfeld C, Kirilovsky D . Specificity of the cyanobacterial orange carotenoid protein: influences of orange carotenoid protein and phycobilisome structures. Plant Physiol. 2013; 164(2):790-804. PMC: 3912106. DOI: 10.1104/pp.113.229997. View

Khan T, Litvin R, Sebelik V, Polivka T . Excited-State Evolution of Keto-Carotenoids after Excess Energy Excitation in the UV Region. Chemphyschem. 2020; 22(5):471-480. DOI: 10.1002/cphc.202000982. View

Pinnola A, Staleva-Musto H, Capaldi S, Ballottari M, Bassi R, Polivka T . Electron transfer between carotenoid and chlorophyll contributes to quenching in the LHCSR1 protein from Physcomitrella patens. Biochim Biophys Acta. 2016; 1857(12):1870-1878. DOI: 10.1016/j.bbabio.2016.09.001. View

van Stokkum I, Gwizdala M, Tian L, Snellenburg J, van Grondelle R, van Amerongen H . A functional compartmental model of the Synechocystis PCC 6803 phycobilisome. Photosynth Res. 2017; 135(1-3):87-102. PMC: 5784004. DOI: 10.1007/s11120-017-0424-5. View

Muller P, Li X, Niyogi K . Non-photochemical quenching. A response to excess light energy. Plant Physiol. 2001; 125(4):1558-66. PMC: 1539381. DOI: 10.1104/pp.125.4.1558. View

Bondanza M, Cupellini L, Faccioli P, Mennucci B . Molecular Mechanisms of Activation in the Orange Carotenoid Protein Revealed by Molecular Dynamics. J Am Chem Soc. 2020; 142(52):21829-21841. PMC: 7775743. DOI: 10.1021/jacs.0c10461. View

Wilson A, Punginelli C, Gall A, Bonetti C, Alexandre M, Routaboul J . A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci U S A. 2008; 105(33):12075-80. PMC: 2575289. DOI: 10.1073/pnas.0804636105. View

10.

Harris D, Tal O, Jallet D, Wilson A, Kirilovsky D, Adir N . Orange carotenoid protein burrows into the phycobilisome to provide photoprotection. Proc Natl Acad Sci U S A. 2016; 113(12):E1655-62. PMC: 4812740. DOI: 10.1073/pnas.1523680113. View

11.

Tian L, van Stokkum I, Koehorst R, Jongerius A, Kirilovsky D, van Amerongen H . Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc. 2011; 133(45):18304-11. DOI: 10.1021/ja206414m. View

12.

Gupta S, Sutter M, Remesh S, Dominguez-Martin M, Bao H, Feng X . X-ray radiolytic labeling reveals the molecular basis of orange carotenoid protein photoprotection and its interactions with fluorescence recovery protein. J Biol Chem. 2019; 294(22):8848-8860. PMC: 6552439. DOI: 10.1074/jbc.RA119.007592. View

13.

Kerfeld C, Sawaya M, Brahmandam V, Cascio D, Ho K, Trevithick-Sutton C . The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure. 2003; 11(1):55-65. DOI: 10.1016/s0969-2126(02)00936-x. View

14.

Adir N . Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res. 2005; 85(1):15-32. DOI: 10.1007/s11120-004-2143-y. View

15.

Tian L, van Stokkum I, Koehorst R, van Amerongen H . Light harvesting and blue-green light induced non-photochemical quenching in two different C-phycocyanin mutants of Synechocystis PCC 6803. J Phys Chem B. 2012; 117(38):11000-6. DOI: 10.1021/jp309570u. View

16.

Balevicius Jr V, Abramavicius D, Polivka T, Galestian Pour A, Hauer J . A Unified Picture of S* in Carotenoids. J Phys Chem Lett. 2016; 7(17):3347-52. PMC: 5011297. DOI: 10.1021/acs.jpclett.6b01455. View

17.

Tian L, Gwizdala M, van Stokkum I, Koehorst R, Kirilovsky D, van Amerongen H . Picosecond kinetics of light harvesting and photoprotective quenching in wild-type and mutant phycobilisomes isolated from the cyanobacterium Synechocystis PCC 6803. Biophys J. 2012; 102(7):1692-700. PMC: 3318131. DOI: 10.1016/j.bpj.2012.03.008. View

18.

Kuznetsova V, Dominguez-Martin M, Bao H, Gupta S, Sutter M, Kloz M . Comparative ultrafast spectroscopy and structural analysis of OCP1 and OCP2 from Tolypothrix. Biochim Biophys Acta Bioenerg. 2019; 1861(2):148120. PMC: 6943196. DOI: 10.1016/j.bbabio.2019.148120. View

19.

Bourcier de Carbon C, Thurotte A, Wilson A, Perreau F, Kirilovsky D . Biosynthesis of soluble carotenoid holoproteins in Escherichia coli. Sci Rep. 2015; 5:9085. PMC: 4358027. DOI: 10.1038/srep09085. View

20.

Niyogi K, Truong T . Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol. 2013; 16(3):307-14. DOI: 10.1016/j.pbi.2013.03.011. View