A comparative study of three signaling forms of the orange carotenoid protein

Photosynthesis Research

Volumn 130, Issue 1-3, 2016, Pages 389-401

  Maksimov, E G ^a   Moldenhauer, M ^b   Shirshin, E A ^a   Parshina, E A ^a   Sluchanko, N N ^c   Klementiev, K E ^a   Tsoraev, G V ^a   Tavraz, N N ^b   Willoweit, M ^b   Schmitt, F J ^b   Breitenbach, J ^d   Sandmann, G ^d   Paschenko, V Z ^a   Friedrich, T ^b   Rubin, A B ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^c BACH INSTITUTE OF BIOCHEMISTRY   (Russian Federation)

^d GOETHE UNIVERSITY   (Germany)

Author keywords

Echinenone; Fluorescence anisotropy; Fluorescence lifetime; Orange carotenoid protein; Protein expression; Synechocystis sp. PCC 6803

Indexed keywords

BACTERIAL PROTEIN; ORANGE CAROTENOID PROTEIN, SYNECHOCYSTIS;

CHEMISTRY; COMPARATIVE STUDY; CYANOBACTERIUM; FLUORESCENCE; FLUORESCENCE POLARIZATION; FLUOROMETRY; ISOLATION AND PURIFICATION; MOLECULAR CLONING; PHYSIOLOGY; RAMAN SPECTROMETRY; SIZE EXCLUSION CHROMATOGRAPHY; SYNECHOCYSTIS;

BACTERIAL PROTEINS; CHROMATOGRAPHY, GEL; CLONING, MOLECULAR; CYANOBACTERIA; FLUORESCENCE; FLUORESCENCE POLARIZATION; FLUOROMETRY; SPECTRUM ANALYSIS, RAMAN; SYNECHOCYSTIS;

EID: 84966560284     PISSN: 01668595     EISSN: 15735079     Source Type: Journal    
DOI: 10.1007/s11120-016-0272-8     Document Type: Article

References (41)

1. Bartalucci G, Coppin J, Fisher S, Hall G, Helliwell JR, Helliwell M, Liaaen-Jensen S (2007) Unravelling the chemical basis of the bathochromic shift in the lobster carapace; new crystal structures of unbound astaxanthin, canthaxanthin and zeaxanthin. Acta Crystallogr B 63:328–337. doi:10.1107/S0108768106052633
2. Berera R, van Stokkum IH, Gwizdala M, Wilson A, Kirilovsky D, van Grondelle R (2012) The photophysics of the orange carotenoid protein, a light-powered molecular switch. J Phys Chem B 116:2568–2574. doi:10.1021/jp2108329
3. Boulay C, Abasova L, Six C, Vass I, Kirilovsky D (2008) Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochim Biophys Acta 1777:1344–1354. doi:10.1016/j.bbabio.2008.07.002
4. Breitenbach J, Gerjets T, Sandmann G (2013) Catalytic properties and reaction mechanism of the CrtO carotenoid ketolase from the cyanobacterium Synechocystis sp. PCC 6803. Arch Biochem Biophys 529:86–91
5. Chabera P, Durchan M, Shih PM, Kerfeld CA, Polivka T (2011) Excited-state properties of the 16 kDa red carotenoid protein from Arthrospira maxima. Biochim Biophys Acta 1807:30–35. doi:10.1016/j.bbabio.2010.08.013
6. Chergui M et al (2013) Comparing the photophysics of the two forms of the Orange carotenoid protein using 2D electronic spectroscopy. EPJ Web of Conferences 41:08008. doi:10.1051/epjconf/20134108008
7. Chib R, Raut S, Sabnis S, Singhal P, Gryczynski Z, Gryczynski I (2014) Associated anisotropy decays of ethidium bromide interacting with DNA. Methods Appl Fluoresc 2(1):015003. doi:10.1088/2050-6120/2/1/015003
8. Cianci M, Rizkallah PJ, Olczak A, Raftery J, Chayen NE, Zagalsky PF, Helliwell JR (2002) The molecular basis of the coloration mechanism in lobster shell: beta-crustacyanin at 3.2-A resolution. Proc Natl Acad Sci USA 99:9795–9800. doi:10.1073/pnas.152088999
9. de Carbon CB, Thurotte A, Wilson A, Perreau F, Kirilovsky D (2015) Biosynthesis of soluble carotenoid holoproteins in Escherichia coli. Sci Rep 5:9085. doi:10.1038/srep09085
10. Demmig-Adams B, Adams WW (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26
11. Denison FC, Gökirmak T, Ferl RJ (2014) Phosphorylation-related modification at the dimer interface of 14-3-3ω dramatically alters monomer interaction dynamics. Arch Biochem Biophys 541:1–12
12. Fernández-González B, Sandmann G, Vioque A (1997) A new type of asymmetrically acting β-carotene ketolase is required for the synthesis of echinenone in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 272:9728–9733
13. Flora K, Brennan JD, Baker GA, Doody MA, Bright FV (1998) Unfolding of acrylodan-labeled human serum albumin probed by steady-state and time-resolved fluorescence methods. Biophys J 75:1084–1096
14. Frank HA, Cogdell RJ (1996) Carotenoids in Photosynthesis. Photochem Photobiol 63:257–264. doi:10.1111/j.1751-1097.1996.tb03022.x
15. Graf M, Bojak A, Deml L, Bieler K, Wolf H, Wagner R (2000) Concerted action of multiple cis-acting sequences is required for Rev dependence of late human immunodeficiency virus type 1 gene expression. J Virol 74:10822–10826
16. Gupta S et al (2015) Local and global structural drivers for the photoactivation of the orange carotenoid protein. Proc Natl Acad Sci USA 112:E5567–E5574. doi:10.1073/pnas.1512240112
17. King JD, Liu H, He G, Orf GS, Blankenship RE (2014) Chemical activation of the cyanobacterial orange carotenoid protein. FEBS Lett 588:4561–4565. doi:10.1016/j.febslet.2014.10.024
18. Kirilovsky D, Kerfeld CA (2013) The Orange Carotenoid Protein: a blue-green light photoactive protein. Photochem Photobiol Sci 12:1135–1143. doi:10.1039/c3pp25406b
19. Kish E, Pinto MM, Kirilovsky D, Spezia R, Robert B (2015) Echinenone vibrational properties: from solvents to the orange carotenoid protein. Biochim Biophys Acta 1847:1044–1054. doi:10.1016/j.bbabio.2015.05.010
20. Lakowicz JR (2013) Principles of fluorescence spectroscopy. Springer, Berlin
21. Leverenz RL, Jallet D, Li MD, Mathies RA, Kirilovsky D, Kerfeld CA (2014) Structural and functional modularity of the orange carotenoid protein: distinct roles for the N- and C-terminal domains in cyanobacterial photoprotection. Plant Cell 26:426–437. doi:10.1105/tpc.113.118588
22. Leverenz RL et al (2015) A 12 Å carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection. Science 348:3
23. Liu WL, Wang ZG, Zheng ZR, Li AH, Su WH (2008) Effect of β-ring rotation on the structures and vibrational spectra of β-carotene: density functional theory analysis. J Phys Chem A 112(42):10580–10585
24. Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342:1104–1107
25. Liu H, Zhang H, King JD, Wolf NR, Prado M, Gross ML, Blankenship RE (2014) Mass spectrometry footprinting reveals the structural rearrangements of cyanobacterial orange carotenoid protein upon light activation. Biochim Biophys Acta 1837:1955–1963. doi:10.1016/j.bbabio.2014.09.004
26. Liu H et al (2016) Dramatic Domain Rearrangements of the Cyanobacterial Orange Carotenoid Protein upon Photoactivation. Biochemistry 55:1003–1009. doi:10.1021/acs.biochem.6b00013
27. Maksimov EG et al (2014) The time course of non-photochemical quenching in phycobilisomes of Synechocystis sp. PCC6803 as revealed by picosecond time-resolved fluorimetry. Biochim Biophys Acta 1837:1540–1547. doi:10.1016/j.bbabio.2014.01.010
28. Maksimov EG et al (2015) The Signaling State of Orange Carotenoid Protein. Biophys J 109:595–607. doi:10.1016/j.bpj.2015.06.052
29. Misawa N et al (1995) Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J Bacteriol 177:6575–6584
30. Niesen FH, Berglund H, Vedadi M (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat Protoc 2(9):2212–2221. doi:10.1038/nprot.2007.321
31. Pascal AA et al (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137
32. Polívka T, Kerfeld CA, Pascher T, Sundström V (2005) Spectroscopic Properties of the Carotenoid 3‘-Hydroxyechinenone in the orange carotenoid protein from the Cyanobacterium Arthrospira maxima. Biochemistry 44:3994–4003. doi:10.1021/bi047473t
33. Salares V, Young N, Bernstein H, Carey P (1979) Mechanisms of spectral shifts in lobster carotenoproteins The resonance raman spectra of ovoverdin and the crustacyanins. Biochim Biophys Acta (BBA) Protein Struct 576:176–191
34. Shakhnovich EI, Finkelstein AV (1989) Theory of cooperative transitions in protein molecules. I. Why denaturation of globular protein is a first-order phase transition. Biopolymers 28:1667–1680. doi:10.1002/bip.360281003
35. Stadnichuk IN, Yanyushin MF, Maksimov EG, Lukashev EP, Zharmukhamedov SK, Elanskaya IV, Paschenko VZ (2012) Site of non-photochemical quenching of the phycobilisome by orange carotenoid protein in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1817:1436–1445. doi:10.1016/j.bbabio.2012.03.023
36. Stadnichuk IN et al (2013) Fluorescence quenching of the phycobilisome terminal emitter LCM from the cyanobacterium Synechocystis sp. PCC 6803 detected in vivo and in vitro. J Photochem Photobiol B 125:137–145. doi:10.1016/j.jphotobiol.2013.05.014
37. Wilson A et al (2010) Structural determinants underlying photoprotection in the photoactive orange carotenoid protein of cyanobacteria. J Biol Chem 285:18364–18375. doi:10.1074/jbc.M110.115709
38. Wilson A, Punginelli C, Couturier M, Perreau F, Kirilovsky D (2011) Essential role of two tyrosines and two tryptophans on the photoprotection activity of the Orange Carotenoid Protein. Biochim Biophys Acta 1807:293–301. doi:10.1016/j.bbabio.2010.12.009
39. Wilson A, Gwizdala M, Mezzetti A, Alexandre M, Kerfeld CA, Kirilovsky D (2012) The essential role of the N-terminal domain of the orange carotenoid protein in cyanobacterial photoprotection: importance of a positive charge for phycobilisome binding. Plant Cell 24:1972–1983. doi:10.1105/tpc.112.096909
40. Yguerabide J, Epstein HF, Stryer L (1970) Segmental flexibility in an antibody molecule. J Mol Biol 51:573–590
41. Zhang H, Liu H, Niedzwiedzki DM, Prado M, Jiang J, Gross ML, Blankenship RE (2014) Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein. Biochemistry 53:13–19. doi:10.1021/bi401539w