Ultrafast Energy Quenching Mechanism of LHCSR3-dependent Photoprotection in Chlamydomonas

Overview

Journal Nat Commun

Specialty Biology

Date 2024 May 24

PMID 38789432

Authors

Mengyuan Zheng

Xiaojie Pang

Ming Chen

Lijin Tian

Affiliations

Soon will be listed here.

Abstract

Photosynthetic organisms have evolved an essential energy-dependent quenching (qE) mechanism to avoid any lethal damages caused by high light. While the triggering mechanism of qE has been well addressed, candidates for quenchers are often debated. This lack of understanding is because of the tremendous difficulty in measuring intact cells using transient absorption techniques. Here, we have conducted femtosecond pump-probe measurements to characterize this photophysical reaction using micro-sized cell fractions of the green alga Chlamydomonas reinhardtii that retain physiological qE function. Combined with kinetic modeling, we have demonstrated the presence of an ultrafast excitation energy transfer (EET) pathway from Chlorophyll a (Chl a) Q to a carotenoid (car) S state, therefore proposing that this carotenoid, likely lutein1, is the quencher. This work has provided an easy-to-prepare qE active thylakoid membrane system for advanced spectroscopic studies and demonstrated that the energy dissipation pathway of qE is evolutionarily conserved from green algae to land plants.

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References

Giovagnetti V, Ware M, Ruban A . Assessment of the impact of photosystem I chlorophyll fluorescence on the pulse-amplitude modulated quenching analysis in leaves of Arabidopsis thaliana. Photosynth Res. 2015; 125(1-2):179-89. DOI: 10.1007/s11120-015-0087-z. 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

Wahadoszamen M, Margalit I, Ara A, van Grondelle R, Noy D . The role of charge-transfer states in energy transfer and dissipation within natural and artificial bacteriochlorophyll proteins. Nat Commun. 2014; 5:5287. PMC: 4255223. DOI: 10.1038/ncomms6287. View

Fan M, Li M, Liu Z, Cao P, Pan X, Zhang H . Crystal structures of the PsbS protein essential for photoprotection in plants. Nat Struct Mol Biol. 2015; 22(9):729-35. DOI: 10.1038/nsmb.3068. View

Troiano J, Perozeni F, Moya R, Zuliani L, Baek K, Jin E . Identification of distinct pH- and zeaxanthin-dependent quenching in LHCSR3 from . Elife. 2021; 10. PMC: 7864637. DOI: 10.7554/eLife.60383. View

De Souza A, Burgess S, Doran L, Hansen J, Manukyan L, Maryn N . Soybean photosynthesis and crop yield are improved by accelerating recovery from photoprotection. Science. 2022; 377(6608):851-854. DOI: 10.1126/science.adc9831. View

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

Morales M, Helias A, Bernard O . Optimal integration of microalgae production with photovoltaic panels: environmental impacts and energy balance. Biotechnol Biofuels. 2019; 12:239. PMC: 6781331. DOI: 10.1186/s13068-019-1579-4. View

Tian L, Nawrocki W, Liu X, Polukhina I, van Stokkum I, Croce R . pH dependence, kinetics and light-harvesting regulation of nonphotochemical quenching in . Proc Natl Acad Sci U S A. 2019; 116(17):8320-8325. PMC: 6486713. DOI: 10.1073/pnas.1817796116. View

10.

Hancock A, Son M, Nairat M, Wei T, Jeuken L, Duffy C . Ultrafast energy transfer between lipid-linked chromophores and plant light-harvesting complex II. Phys Chem Chem Phys. 2021; 23(35):19511-19524. PMC: 8442836. DOI: 10.1039/d1cp01628h. View

11.

Mukherjee A . State Transition Regulation in . Plant Physiol. 2020; 183(4):1418-1419. PMC: 7401128. DOI: 10.1104/pp.20.00814. View

12.

Peers G, Truong T, Ostendorf E, Busch A, Elrad D, Grossman A . An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature. 2009; 462(7272):518-21. DOI: 10.1038/nature08587. View

13.

Walker J . The bicinchoninic acid (BCA) assay for protein quantitation. Methods Mol Biol. 1994; 32:5-8. DOI: 10.1385/0-89603-268-X:5. View

14.

Berera R, van Grondelle R, Kennis J . Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems. Photosynth Res. 2009; 101(2-3):105-18. PMC: 2744833. DOI: 10.1007/s11120-009-9454-y. View

15.

Yoneda Y, Katayama T, Nagasawa Y, Miyasaka H, Umena Y . Dynamics of Excitation Energy Transfer Between the Subunits of Photosystem II Dimer. J Am Chem Soc. 2016; 138(36):11599-605. DOI: 10.1021/jacs.6b04316. View

16.

Liguori N, Roy L, Opacic M, Durand G, Croce R . Regulation of light harvesting in the green alga Chlamydomonas reinhardtii: the C-terminus of LHCSR is the knob of a dimmer switch. J Am Chem Soc. 2013; 135(49):18339-42. DOI: 10.1021/ja4107463. View

17.

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

18.

Giera W, Szewczyk S, McConnell M, Snellenburg J, Redding K, van Grondelle R . Excitation dynamics in Photosystem I from Chlamydomonas reinhardtii. Comparative studies of isolated complexes and whole cells. Biochim Biophys Acta. 2014; 1837(10):1756-68. DOI: 10.1016/j.bbabio.2014.06.004. View

19.

Staleva H, Komenda J, Shukla M, Slouf V, Kana R, Polivka T . Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat Chem Biol. 2015; 11(4):287-91. DOI: 10.1038/nchembio.1755. View

20.

Croce R, van Amerongen H . Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy. Science. 2020; 369(6506). DOI: 10.1126/science.aay2058. View