OCP-FRP Protein Complex Topologies Suggest a Mechanism for Controlling High Light Tolerance in Cyanobacteria

Overview

Journal Nat Commun

Specialty Biology

Date 2018 Sep 26

PMID 30250028

Citations 12

Authors

Nikolai N Sluchanko

Yury B Slonimskiy

Evgeny A Shirshin

Marcus Moldenhauer

Thomas Friedrich

Eugene G Maksimov

Affiliations

Soon will be listed here.

Abstract

In cyanobacteria, high light photoactivates the orange carotenoid protein (OCP) that binds to antennae complexes, dissipating energy and preventing the destruction of the photosynthetic apparatus. At low light, OCP is efficiently deactivated by a poorly understood action of the dimeric fluorescence recovery protein (FRP). Here, we engineer FRP variants with defined oligomeric states and scrutinize their functional interaction with OCP. Complemented by disulfide trapping and chemical crosslinking, structural analysis in solution reveals the topology of metastable complexes of OCP and the FRP scaffold with different stoichiometries. Unable to tightly bind monomeric FRP, photoactivated OCP recruits dimeric FRP, which subsequently monomerizes giving 1:1 complexes. This could be facilitated by a transient OCP-2FRP-OCP complex formed via the two FRP head domains, significantly improving FRP efficiency at elevated OCP levels. By identifying key molecular interfaces, our findings may inspire the design of optically triggered systems transducing light signals into protein-protein interactions.

Citing Articles

Structure and function of the light-protective orange carotenoid protein families.

Garcia-Oneto T, Moyano-Bellido C, Dominguez-Martin M Curr Res Struct Biol. 2024; 7:100141.

PMID: 38736459 PMC: 11087925. DOI: 10.1016/j.crstbi.2024.100141.

Insights into the molecular mechanism of yellow cuticle coloration by a chitin-binding carotenoprotein in gregarious locusts.

Egorkin N, Dominnik E, Maksimov E, Sluchanko N Commun Biol. 2024; 7(1):448.

PMID: 38605243 PMC: 11009388. DOI: 10.1038/s42003-024-06149-x.

Solution Structures of Two Different FRP-OCP Complexes as Revealed via SEC-SANS.

Hajizadeh M, Golub M, Moldenhauer M, Matsarskaia O, Martel A, Porcar L Int J Mol Sci. 2024; 25(5).

PMID: 38474026 PMC: 10932109. DOI: 10.3390/ijms25052781.

Structural basis for the ligand promiscuity of the neofunctionalized, carotenoid-binding fasciclin domain protein AstaP.

Kornilov F, Slonimskiy Y, Lunegova D, Egorkin N, Savitskaya A, Kleymenov S Commun Biol. 2023; 6(1):471.

PMID: 37117801 PMC: 10147662. DOI: 10.1038/s42003-023-04832-z.

Fortuitously compatible protein surfaces primed allosteric control in cyanobacterial photoprotection.

Steube N, Moldenhauer M, Weiland P, Saman D, Kilb A, Ramirez Rojas A Nat Ecol Evol. 2023; 7(5):756-767.

PMID: 37012377 PMC: 10172135. DOI: 10.1038/s41559-023-02018-8.

References

Whitmore L, Wallace B . DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 2004; 32(Web Server issue):W668-73. PMC: 441509. DOI: 10.1093/nar/gkh371. View

Sonani R, Gardiner A, Rastogi R, Cogdell R, Robert B, Madamwar D . Site, trigger, quenching mechanism and recovery of non-photochemical quenching in cyanobacteria: recent updates. Photosynth Res. 2018; 137(2):171-180. DOI: 10.1007/s11120-018-0498-8. View

Wilson A, Ajlani G, Verbavatz J, Vass I, Kerfeld C, Kirilovsky D . A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell. 2006; 18(4):992-1007. PMC: 1425857. DOI: 10.1105/tpc.105.040121. View

Blanchet C, Spilotros A, Schwemmer F, Graewert M, Kikhney A, Jeffries C . Versatile sample environments and automation for biological solution X-ray scattering experiments at the P12 beamline (PETRA III, DESY). J Appl Crystallogr. 2015; 48(Pt 2):431-443. PMC: 4379436. DOI: 10.1107/S160057671500254X. View

Lu Y, Liu H, Saer R, Zhang H, Meyer C, Li V . Native Mass Spectrometry Analysis of Oligomerization States of Fluorescence Recovery Protein and Orange Carotenoid Protein: Two Proteins Involved in the Cyanobacterial Photoprotection Cycle. Biochemistry. 2016; 56(1):160-166. PMC: 5369232. DOI: 10.1021/acs.biochem.6b01094. View

Thurotte A, Bourcier de Carbon C, Wilson A, Talbot L, Cot S, Lopez-Igual R . The cyanobacterial Fluorescence Recovery Protein has two distinct activities: Orange Carotenoid Protein amino acids involved in FRP interaction. Biochim Biophys Acta Bioenerg. 2017; 1858(4):308-317. DOI: 10.1016/j.bbabio.2017.02.003. View

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

Thurotte A, Lopez-Igual R, Wilson A, Comolet L, Bourcier de Carbon C, Xiao F . Regulation of Orange Carotenoid Protein Activity in Cyanobacterial Photoprotection. Plant Physiol. 2015; 169(1):737-47. PMC: 4577420. DOI: 10.1104/pp.15.00843. View

Baker N, Sept D, Joseph S, Holst M, McCammon J . Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A. 2001; 98(18):10037-41. PMC: 56910. DOI: 10.1073/pnas.181342398. View

10.

Gwizdala M, Wilson A, Kirilovsky D . In vitro reconstitution of the cyanobacterial photoprotective mechanism mediated by the Orange Carotenoid Protein in Synechocystis PCC 6803. Plant Cell. 2011; 23(7):2631-43. PMC: 3226224. DOI: 10.1105/tpc.111.086884. View

11.

Sutter M, Wilson A, Leverenz R, Lopez-Igual R, Thurotte A, Salmeen A . Crystal structure of the FRP and identification of the active site for modulation of OCP-mediated photoprotection in cyanobacteria. Proc Natl Acad Sci U S A. 2013; 110(24):10022-7. PMC: 3683793. DOI: 10.1073/pnas.1303673110. View

12.

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

13.

Lu Y, Liu H, Saer R, Li V, Zhang H, Shi L . A Molecular Mechanism for Nonphotochemical Quenching in Cyanobacteria. Biochemistry. 2017; 56(22):2812-2823. PMC: 5623595. DOI: 10.1021/acs.biochem.7b00202. View

14.

Gupta S, Guttman M, Leverenz R, Zhumadilova K, Pawlowski E, Petzold C . Local and global structural drivers for the photoactivation of the orange carotenoid protein. Proc Natl Acad Sci U S A. 2015; 112(41):E5567-74. PMC: 4611662. DOI: 10.1073/pnas.1512240112. View

15.

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

16.

Stadnichuk I, Yanyushin M, Maksimov E, Lukashev E, Zharmukhamedov S, Elanskaya I . Site of non-photochemical quenching of the phycobilisome by orange carotenoid protein in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta. 2012; 1817(8):1436-45. DOI: 10.1016/j.bbabio.2012.03.023. View

17.

Svergun D, Petoukhov M, Koch M . Determination of domain structure of proteins from X-ray solution scattering. Biophys J. 2001; 80(6):2946-53. PMC: 1301478. DOI: 10.1016/S0006-3495(01)76260-1. View

18.

Shcherbakova D, Shemetov A, Kaberniuk A, Verkhusha V . Natural photoreceptors as a source of fluorescent proteins, biosensors, and optogenetic tools. Annu Rev Biochem. 2015; 84:519-50. PMC: 4681293. DOI: 10.1146/annurev-biochem-060614-034411. View

19.

Valentini E, Kikhney A, Previtali G, Jeffries C, Svergun D . SASBDB, a repository for biological small-angle scattering data. Nucleic Acids Res. 2014; 43(Database issue):D357-63. PMC: 4383894. DOI: 10.1093/nar/gku1047. View

20.

Maksimov E, Shirshin E, Sluchanko N, Zlenko D, Parshina E, Tsoraev G . The Signaling State of Orange Carotenoid Protein. Biophys J. 2015; 109(3):595-607. PMC: 4572496. DOI: 10.1016/j.bpj.2015.06.052. View