Photosynthesis Research

, Volume 137, Issue 2, pp 171–180 | Cite as

Site, trigger, quenching mechanism and recovery of non-photochemical quenching in cyanobacteria: recent updates

  • Ravi R. Sonani
  • Alastair Gardiner
  • Rajesh P. Rastogi
  • Richard Cogdell
  • Bruno Robert
  • Datta Madamwar
Critical Review


Cyanobacteria exhibit a novel form of non-photochemical quenching (NPQ) at the level of the phycobilisome. NPQ is a process that protects photosystem II (PSII) from possible highlight-induced photo-damage. Although significant advancement has been made in understanding the NPQ, there are still some missing details. This critical review focuses on how the orange carotenoid protein (OCP) and its partner fluorescence recovery protein (FRP) control the extent of quenching. What is and what is not known about the NPQ is discussed under four subtitles; where does exactly the site of quenching lie? (site), how is the quenching being triggered? (trigger), molecular mechanism of quenching (quenching) and recovery from quenching. Finally, a recent working model of NPQ, consistent with recent findings, is been described.


Cyanobacteria Non-photochemical quenching Orange carotenoid protein Phycobilisome Fluorescence recovery protein 



Ravi R Sonani is deeply thankful to the Department of Science and Technology (DST), New Delhi, Indo-French Centre for the Promotion of Advance Research (IFCPAR), New Delhi and British Council for the financial support. Datta Madamwar acknowledges University Grants Commission (UGC), New Delhi for BSR Faculty Grant.

Compliance with ethical standards

Conflict of interest

The authors report no conflicts of interest.


  1. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85(1):15–32PubMedGoogle Scholar
  2. Adir N (2008) Structure of the phycobilisome antennae in cyanobacteria and red algae. Photosynth Protein Complex 243–274Google Scholar
  3. Bandara S, Ren Z, Lu L, Zeng X, Shin H, Zhao K-H, Yang X (2017) Photoactivation mechanism of a carotenoid-based photoreceptor. Proc Natl Acad Sci 114(24):6286–6291PubMedGoogle Scholar
  4. Bao H, Melnicki MR, Kerfeld CA (2017a) Structure and functions of orange carotenoid protein homologs in cyanobacteria. Curr Opin Plant Biol 37:1–9PubMedGoogle Scholar
  5. Bao H, Melnicki MR, Pawlowski EG, Sutter M, Agostoni M, Lechno-Yossef S, Cai F, Montgomery BL, Kerfeld CA (2017b) Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria. Nat Plants 3(8):17089PubMedGoogle Scholar
  6. Berera R, van Stokkum IH, Gwizdala M, Wilson Al, Kirilovsky D, van Grondelle R (2012) The photophysics of the orange carotenoid protein, a light-powered molecular switch. J Phys Chem B 116(8):2568–2574PubMedGoogle Scholar
  7. Berera R, Gwizdala M, van Stokkum IH, Kirilovsky D, van Grondelle R (2013) Excited states of the inactive and active forms of the orange carotenoid protein. J Phys Chem B 117(31):9121–9128PubMedGoogle Scholar
  8. Bode S, Quentmeier CC, Liao P-N, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci 106(30):12311–12316PubMedGoogle Scholar
  9. Boulay C, Wilson A, D’Haene S, Kirilovsky D (2010) Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria. Proc Natl Acad Sci 107(25):11620–11625PubMedGoogle Scholar
  10. El Bissati K, Delphin E, Murata N, Etienne A-L, Kirilovsky D (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457(3):229–242PubMedGoogle Scholar
  11. Franck J, Gaffron H (1941) Photosynthesis, facts and interpretations. Adv Enzymol Relat Areas Mol Biol 1:199–262Google Scholar
  12. Gantt E, Lipschultz C (1973) Energy transfer in phycobilisomes from phycoerythrin to allophycocyanin. Biochim Biophys Acta 292(3):858–861PubMedGoogle Scholar
  13. Glazer AN (1984) Phycobilisome a macromolecular complex optimized for light energy transfer. Biochim Biophys Acta 768(1):29–51Google Scholar
  14. Gupta S, Guttman M, Leverenz RL, Zhumadilova K, Pawlowski EG, Petzold CJ, Lee KK, Ralston CY, Kerfeld CA (2015) Local and global structural drivers for the photoactivation of the orange carotenoid protein. Proc Natl Acad Sci 112(41):E5567–E5574PubMedGoogle Scholar
  15. Gwizdala M, Wilson A, Kirilovsky D (2011) In vitro reconstitution of the cyanobacterial photoprotective mechanism mediated by the orange carotenoid protein in Synechocystis PCC 6803. Plant Cell 23(7):2631–2643PubMedPubMedCentralGoogle Scholar
  16. Gwizdala M, Wilson A, Omairi-Nasser A, Kirilovsky D (2013) Characterization of the Synechocystis PCC 6803 fluorescence recovery protein involved in photoprotection. Biochim Biophys Acta 1827(3):348–354PubMedGoogle Scholar
  17. Harris D, Tal O, Jallet D, Wilson A, Kirilovsky D, Adir N (2016) Orange carotenoid protein burrows into the phycobilisome to provide photoprotection. Proc Natl Acad Sci 113(12):E1655–E1662PubMedGoogle Scholar
  18. Holt TK, Krogmann DW (1981) A carotenoid-protein from cyanobacteria. Biochim Biophys Acta 637(3):408–414Google Scholar
  19. Holt NE, Zigmantas D, Valkunas L, Li X-P, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307(5708):433–436PubMedGoogle Scholar
  20. Jallet D, Gwizdala M, Kirilovsky D (2012) ApcD, ApcF and ApcE are not required for the orange carotenoid protein related phycobilisome fluorescence quenching in the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta 1817(8):1418–1427PubMedGoogle Scholar
  21. Kerfeld CA, Sawaya MR, Brahmandam V, Cascio D, Ho KK, Trevithick-Sutton CC, Krogmann DW, Yeates TO (2003) The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure 11(1):55–65PubMedGoogle Scholar
  22. King JD, Liu H, He G, Orf GS, Blankenship RE (2014) Chemical activation of the cyanobacterial orange carotenoid protein. FEBS Lett 588(24):4561–4565PubMedGoogle Scholar
  23. Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93(1–3):7PubMedGoogle Scholar
  24. Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817(1):158–166PubMedGoogle Scholar
  25. Kish E, Pinto MMM, Kirilovsky D, Spezia R, Robert B (2015) Echinenone vibrational properties: from solvents to the orange carotenoid protein. Biochim Biophys Acta 1847(10):1044–1054PubMedGoogle Scholar
  26. Kuzminov F, Karapetyan N, Rakhimberdieva M, Elanskaya I, Gorbunov M, Fadeev V (2012) Investigation of OCP-triggered dissipation of excitation energy in PSI/PSII-less Synechocystis sp. PCC 6803 mutant using non-linear laser fluorimetry. Biochim Biophys Acta 1817(7):1012–1021PubMedGoogle Scholar
  27. Leverenz RL, Jallet D, 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(1):426–437PubMedPubMedCentralGoogle Scholar
  28. Leverenz RL, Sutter M, Wilson A, Gupta S, Thurotte A, de Carbon CB, Petzold CJ, Ralston C, Perreau F, Kirilovsky D (2015) A 12 Å carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection. Science 348(6242):1463–1466PubMedGoogle Scholar
  29. Liu H, Zhang H, Orf GS, Lu Y, Jiang J, King JD, Wolf NR, Gross ML, Blankenship RE (2016) Dramatic domain rearrangements of the cyanobacterial orange carotenoid protein upon photoactivation. Biochemistry 55(7):1003–1009PubMedPubMedCentralGoogle Scholar
  30. Lu Y, Liu H, Saer RG, Zhang H, Meyer CM, Li VL, Shi L, King JD, Gross ML, Blankenship RE (2016) Native mass spectrometry analysis of oligomerization states of fluorescence recovery protein and orange carotenoid protein: two proteins involved in the cyanobacterial photoprotection cycle. Biochemistry 56(1):160–166PubMedPubMedCentralGoogle Scholar
  31. Lu Y, Liu H, Saer R, Li VL, Zhang H, Shi L, Goodson C, Gross ML, Blankenship RE (2017) A molecular mechanism for nonphotochemical quenching in cyanobacteria. Biochemistry 56(22):2812–2823PubMedPubMedCentralGoogle Scholar
  32. MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124(2):311–334PubMedGoogle Scholar
  33. Maksimov EG, Shirshin EA, Sluchanko NN, Zlenko DV, Parshina EY, Tsoraev GV, Klementiev KE, Budylin GS, Schmitt F-J, Friedrich T (2015) The signaling state of orange carotenoid protein. Biophys J 109(3):595–607PubMedPubMedCentralGoogle Scholar
  34. Maksimov EG, Sluchanko NN, Slonimskiy YB, Mironov KS, Klementiev KE, Moldenhauer M, Friedrich T, Los DA, Paschenko VZ, Rubin AB (2017a) The unique protein-to-protein carotenoid transfer mechanism. Biophys J 113(2):402–414PubMedGoogle Scholar
  35. Maksimov EG, Sluchanko NN, Slonimskiy YB, Slutskaya E, Stepanov A, Argentova-Stevens A, Shirshin E, Tsoraev G, Klementiev K, Slatinskaya O (2017b) The photocycle of orange carotenoid protein conceals distinct intermediates and asynchronous changes in the carotenoid and protein components. Sci Rep 7(1):15548PubMedPubMedCentralGoogle Scholar
  36. Maksimov EG, Sluchanko NN, Slonimskiy YB, Stepanov AV, Shirshin EA, Tsoraev GV, Klementiev KE, Slatinskaya OV, Lukashev EP, Friedrich T (2017c) The photocycle of orange carotenoid protein conceals distinct intermediates and asynchronous changes in the carotenoid and protein components. bioRxiv 167478Google Scholar
  37. McGregor A, Klartag M, David L, Adir N (2008) Allophycocyanin trimer stability and functionality are primarily due to polar enhanced hydrophobicity of the phycocyanobilin binding pocket. J Mol Biol 384(2):406–421PubMedGoogle Scholar
  38. Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4(4):130–135PubMedGoogle Scholar
  39. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177(4):272–280Google Scholar
  40. Moldenhauer M, Sluchanko NN, Buhrke D, Zlenko DV, Tavraz NN, Schmitt F-J, Hildebrandt P, Maksimov EG, Friedrich T (2017a) Assembly of photoactive orange carotenoid protein from its domains unravels a carotenoid shuttle mechanism. Photosynth Res 133(1–3):327–341PubMedGoogle Scholar
  41. Moldenhauer M, Sluchanko NN, Tavraz NN, Junghans C, Buhrke D, Willoweit M, Chiappisi L, Schmitt F-J, Vukojević V, Shirshin EA (2017b) Interaction of the signaling state analog and the apoprotein form of the orange carotenoid protein with the fluorescence recovery protein. Photosynth Res:1–15Google Scholar
  42. Mori Y (2016) Computational study on the color change of 3′-hydroxyechinenone in the orange carotenoid protein. Chem Phys Lett 652:184–189Google Scholar
  43. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125(4):1558–1566PubMedPubMedCentralGoogle Scholar
  44. Niedzwiedzki DM, Liu H, Blankenship RE (2014) Excited state properties of 3′-hydroxyechinenone in solvents and in the orange carotenoid protein from Synechocystis sp. PCC 6803. J Phys Chem B 118(23):6141–6149PubMedGoogle Scholar
  45. 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(10):3994–4003PubMedGoogle Scholar
  46. Punginelli C, Wilson A, Routaboul J-M, Kirilovsky D (2009) Influence of zeaxanthin and echinenone binding on the activity of the orange carotenoid protein. Biochim Biophys Acta 1787(4):280–288PubMedGoogle Scholar
  47. Rakhimberdieva MG, Stadnichuk IN, Elanskaya IV, Karapetyan NV (2004) Carotenoid-induced quenching of the phycobilisome fluorescence in photosystem II-deficient mutant of Synechocystis sp. FEBS Lett 574(1–3):85–88PubMedGoogle Scholar
  48. Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photo damage. Plant Physiol 170(4):1903–1916PubMedPubMedCentralGoogle Scholar
  49. Ruban AV, Berera R, Ilioaia C, Van Stokkum IH, Kennis JT, Pascal AA, Van Amerongen H, Robert B, Horton P, Van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450(7169):575–578PubMedGoogle Scholar
  50. Scott M, Vasil’ev S, McCollum C, Crozier C, Espie G, Bruce D (2005) Blue light induced fluorescence quenching in a PSII-less mutant of Synechocystis PCC 6803. In: van der Est A, Bruce D (eds) Photosynthesis: fundamental aspects to global perspectives. Elsevier Science Publishers, Amsterdam, pp 577–579Google Scholar
  51. Scott M, McCollum C, Vasil’ev S, Crozier C, Espie GS, Krol M, Huner NP, Bruce D (2006) Mechanism of the down regulation of photosynthesis by blue light in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 45(29):8952–8958PubMedGoogle Scholar
  52. Singh NK, Sonani RR, Rastogi RP, Madamwar D (2015) The phycobilisomes: an early requisite for efficient photosynthesis in cyanobacteria. EXCLI J 14:268PubMedPubMedCentralGoogle Scholar
  53. Sluchanko NN, Klementiev KE, Shirshin EA, Tsoraev GV, Friedrich T, Maksimov EG (2017a) The purple Trp288Ala mutant of Synechocystis OCP persistently quenches phycobilisome fluorescence and tightly interacts with FRP. Biochim Biophys Acta 1858(1):1–11PubMedGoogle Scholar
  54. Sluchanko NN, Slonimskiy YB, Moldenhauer M, Friedrich T, Maksimov EG (2017b) Deletion of the short N-terminal extension in OCP reveals the main site for FRP binding. FEBS LettGoogle Scholar
  55. Stadnichuk IN, Yanyushin MF, Bernát G, Zlenko DV, Krasilnikov PM, Lukashev EP, Maksimov EG, Paschenko VZ (2013) Fluorescence quenching of the phycobilisome terminal emitter L CM from the cyanobacterium Synechocystis sp. PCC 6803 detected in vivo and in vitro. J Photochem Photobiol B 125:137–145PubMedGoogle Scholar
  56. Stadnichuk IN, Krasilnikov PM, Zlenko DV, Freidzon AY, Yanyushin MF, Rubin AB (2015) Electronic coupling of the phycobilisome with the orange carotenoid protein and fluorescence quenching. Photosynth Res 124(3):315–335PubMedGoogle Scholar
  57. Sutter M, Wilson A, Leverenz RL, Lopez-Igual R, Thurotte A, Salmeen AE, Kirilovsky D, Kerfeld CA (2013) Crystal structure of the FRP and identification of the active site for modulation of OCP-mediated photoprotection in cyanobacteria. Proc Natl Acad Sci 110(24):10022–10027PubMedGoogle Scholar
  58. Thurotte A, de Carbon CB, Wilson A, Talbot L, Cot S, López-Igual R, Kirilovsky D (2017) The cyanobacterial fluorescence recovery protein has two distinct activities: orange carotenoid protein amino acids involved in FRP interaction. Biochim Biophys Acta 1858(4):308–317PubMedGoogle Scholar
  59. Tian L, van Stokkum IH, Koehorst RB, Jongerius A, Kirilovsky D, van Amerongen H (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133(45):18304–18311PubMedGoogle Scholar
  60. Tian L, Gwizdala M, van Stokkum IH, Koehorst RB, Kirilovsky D, van Amerongen H (2012) Picosecond kinetics of light harvesting and photoprotective quenching in wild-type and mutant phycobilisomes isolated from the cyanobacterium Synechocystis PCC 6803. Biophys J 102(7):1692–1700PubMedPubMedCentralGoogle Scholar
  61. Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18(4):992–1007PubMedPubMedCentralGoogle Scholar
  62. Wilson A, Punginelli C, Gall A, Bonetti C, Alexandre M, Routaboul J-M, Kerfeld CA, Van Grondelle R, Robert B, Kennis JT (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci 105(33):12075–12080PubMedGoogle Scholar
  63. 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(3):293–301PubMedGoogle Scholar
  64. Zhang H, Liu H, Niedzwiedzki DM, Prado M, Jiang J, Gross ML, Blankenship RE (2013) Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein. Biochemistry 53(1):13–19PubMedPubMedCentralGoogle Scholar
  65. Zlenko DV, Krasilnikov PM, Stadnichuk IN (2016) Role of inter-domain cavity in the attachment of the orange carotenoid protein to the phycobilisome core and to the fluorescence recovery protein. J Biomol Struct Dyn 34(3):486–496PubMedGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Post-Graduate Department of BiosciencesSardar Patel UniversityAnandIndia
  2. 2.Institute of Molecular, Cell and System BiologyUniversity of GlasgowGlasgowUK
  3. 3.CEA, Institute of Biology and Technology of Saclay, CNRSGif/YvetteFrance
  4. 4.School of SciencesP. P. Savani UniversitySuratIndia

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