Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism

  • Diana Kirilovsky
Original Paper


Plants and algae have developed multiple protective mechanisms to survive under high light conditions. Thermal dissipation of excitation energy in the membrane-bound chlorophyll-antenna of photosystem II (PSII) decreases the energy arriving at the reaction center and thus reduces the generation of toxic photo-oxidative species. This process results in a decrease of PSII-related fluorescence emission, known as non-photochemical quenching (NPQ). It has always been assumed that cyanobacteria, the progenitor of the chloroplast, lacked an equivalent photoprotective mechanism. Recently, however, evidence has been presented for the existence of at least three distinct mechanisms for dissipating excess absorbed energy in cyanobacteria. One of these mechanisms, characterized by a blue-light-induced fluorescence quenching, is related to the phycobilisomes, the extramembranal antenna of cyanobacterial PSII. In this photoprotective mechanism the soluble carotenoid-binding protein (OCP) encoded by the slr1963 gene in Synechocystis sp. PCC 6803, of previously unknown function, plays an essential role. The amount of energy transferred from the phycobilisomes to the photosystems is reduced and the OCP acts as the photoreceptor and as the mediator of this antenna-related process. These are novel roles for a soluble carotenoid protein.


Cyanobacteria Non-photochemical-quenching Orange-carotenoid-protein Photoprotection Phycobilisomes 





Green fluorescence protein


Light harvesting complex II




Orange carotenoid protein




Photosystem I


Photosystem II



Many thanks to Dr A. William Rutherford for stimulating discussions and critical reading of this manuscript and to Dr Cheryl Kerfeld, Dr Ghada Ajlani and Dr Imre Vass for stimulating discussions. The work was partially supported by EU network INTRO2.


  1. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome : reconstructing a giant. Photosynth Res 85:15–32CrossRefPubMedGoogle Scholar
  2. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335PubMedCrossRefGoogle Scholar
  3. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134CrossRefPubMedGoogle Scholar
  4. Andrizhiyevskaya EG, Schwabe TM, Germano M, D’Haene S, Kruip J, van Grondelle R, Dekker JP (2002) Spectroscopic properties of PSI-IsiA supercomplexes of the cyanobacterium Synechococcus PCC 7942. Biochim Biophys Acta 1556:265–272CrossRefPubMedGoogle Scholar
  5. Bailey S, Mann N, Robinson C, Scanlan DJ (2005) The occurrence of rapidly reversible non-photochemical quenching of chlorophyll a fluorescence in cyanobacteria. FEBS Lett 579:275–280CrossRefPubMedGoogle Scholar
  6. Bibby TS, Nield J, Barber J (2001) Iron deficiency induces the formation of an antenna ring around trimeric photosystem I in cyanobacteria. Nature 412:743–745CrossRefPubMedGoogle Scholar
  7. Boekema EJ, Hifney A, Yakushevska AE, Piotrowski M, Keegstra W, Berry S, Michel KP, Pistorius EK, Kruip J (2001) A giant chlorophyll-protein complex induced by iron-deficiency in cyanobacteria. Nature 412:745–748CrossRefPubMedGoogle Scholar
  8. Burnap R, Troyan T, Sherman L (1993) The highly abundant chlorophyll-protein of iron-deficient Synechococcus sp PCC 7942 (CP43′) is encoded by the isiA gene. Plant Physiol 103:893–902CrossRefPubMedGoogle Scholar
  9. Cadoret J-C, Demoulière R, Lavaud J, van Gorkom H, Houmard J, Etienne A-L (2004) Dissipation of excess energy triggered by blue-light in cyanobacteria with CP43’ (isiA). Biochim Biophys Acta 1659:100–104CrossRefPubMedGoogle Scholar
  10. Campbell D, Hurry V, Clarke A, Gustafsson P, Oquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 6:667–683Google Scholar
  11. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24CrossRefGoogle Scholar
  12. Diverse-Pierluissi M, Krogmann DW (1988) A zeaxanthin protein from Anacystis nidulans. Biochim Biophys Acta 933:372–377CrossRefGoogle Scholar
  13. Dominy PJ, Williams WP (1987) The role of respiratory electron flow in the control of excitation energy distribution in blue-green algae. Biochim Biophys Acta 892:264–274CrossRefGoogle Scholar
  14. 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 1457:229–242CrossRefPubMedGoogle Scholar
  15. El Bissati K, Kirilovsky D (2001) Regulation of psbA and psaE expression by light quality in Synechocystis species PCC 6803. A redox control mechanism. Plant Physiol 125:1988–2000CrossRefPubMedGoogle Scholar
  16. Fork DC, Satoh K (1983) State1-State2 transitions in the thermophilic blue-green algae (cyanobacterium) Synechococcus lividus. Photochem Photobiol 37:421–427Google Scholar
  17. Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, Hagemann M (2006). Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. PCC 6803. Proteomics 6:2733–2745CrossRefPubMedGoogle Scholar
  18. Havaux M, Guedeney G, He Q, Grossman AR (2002) Elimination of high-light-inducible polypeptides related to eukaryotic chlorophyll a:b-binding proteins results in aberrant photoacclimation in Synechocystis PCC 6803. Biochim Biophys Acta 1557: 21–33Google Scholar
  19. Havaux M, Guedeney G, Hagemann MR, Yeremenko N, Matthijs H, Jeanjean R (2005) The chlorophyll-binding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress. FEBS Lett 579: 2289–2293CrossRefPubMedGoogle Scholar
  20. Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793–806CrossRefPubMedGoogle Scholar
  21. Holt TK, Krogmann DW (1981) A carotenoid protein from cyanobacteria. Biochim Biophys Acta 637:408–414CrossRefGoogle Scholar
  22. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684CrossRefPubMedGoogle Scholar
  23. Ihalainen J, D’Haene S, Yeremenko N, van Roon H, Arteni A, Boekema E, van Grondelle R, Matthijs H, Dekker J (2005) Aggregates of the chlorophyll-binding protein IsiA (CP43’) dissipate energy in cyanobacteria. Biochemistry 44:10846–10853CrossRefPubMedGoogle Scholar
  24. Jeanjean R, Zuther E, Yeremenko N, van Roon H, Arteni A, Boekema E, van Grondelle R, Matthijs H, Dekker J (2003) A photosystem I psaFJ-null mutant of the cyanobacterium Synechocystis 6803 expresses the isiAB operon under iron replete conditions. FEBS Lett 549:52–56CrossRefPubMedGoogle Scholar
  25. Joshua S, Mullineaux C (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135:2112–2119CrossRefPubMedGoogle Scholar
  26. Joshua S, Bailey S, Mann N, Mullineaux C (2005) Involvement of phycobilisome diffusion in energy quenching in cyanobacteria. Plant Physiol 138:1577–1585CrossRefPubMedGoogle Scholar
  27. Kerfeld C, Sawaya M , Brahmandam V, Cascio D, Ho K, Trevithick-Sutton C , Krogmann DW, Yeates TO (2003) The crystal structure of a cyanobacterial water-soluble protein. Structure 11:1–20CrossRefGoogle Scholar
  28. Kerfeld CA (2004) Structure and function of the water-soluble carotenoid-binding proteins in cyanobacteria. Photosynth Res 81:215–225CrossRefPubMedGoogle Scholar
  29. Kerfeld CA (2004) Water-soluble carotenoid proteins of cyanobacteria. Arch Biochem Biophys 430:2–9CrossRefPubMedGoogle Scholar
  30. Laudenbach D, Straus N (1988) Characterization of a cyanobacterial iron stress-induced gene similar to psbC. J Bacteriol 170:5018–5026PubMedGoogle Scholar
  31. MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334CrossRefPubMedGoogle Scholar
  32. Melkozernov AN, Bibby TS, Lin S, Barber J, Blankenship RE (2003) Time-resolved absorption and emission show that the CP43′ antenna ring of iron-stressed Synechocystis sp PCC 6803 is efficiently coupled to the photosystem I reaction center core. Biochemistry 42:3893–3903CrossRefPubMedGoogle Scholar
  33. Müller P, Li X-P, Niyogi K (2001) Non-phochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedGoogle Scholar
  34. Mullineaux C (1992) Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium. Biochim Biophys Acta 1100:285–292Google Scholar
  35. Mullineaux C (1993) Inhibition by phosphate of light state transitiona in cyanobacterial cells. Photosynth Res 38:135–140CrossRefGoogle Scholar
  36. Mullineaux C, Allen JF (1986) The state 2 transition in the cyanobacterium Synechococcus 6301 can be driven by respiratory electron flow into the plastoquinone pool. FEBS Lett 205:155–160CrossRefGoogle Scholar
  37. Mullineaux C, Allen JF (1990) State1-state2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystem I and II. Photosynth Res 23:297–311CrossRefGoogle Scholar
  38. Mullineaux C, Sarcina S (2002) Probing the dynamics of photosynthetic membranes with fluorescence recovery after photobleaching. Trends Plant Sci 7:237–240CrossRefPubMedGoogle Scholar
  39. Niyogi K (1999) Photoprotection revisited: genetic and molecular approaches. Ann Rev Plant Mol Biol 50:333–359CrossRefGoogle Scholar
  40. Polivka 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 44:3994–4003CrossRefPubMedGoogle Scholar
  41. Prasil O, Adir N, Ohad I (1992) Dynamics of photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J (ed) The photosystems: structure, function and molecular biology. Elsevier Science Publishers, Amsterdam, pp 295–348Google Scholar
  42. Rakhimberdieva M, Boichenko VA, Karapetyan N, Stadnichuk I (2001) Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis. Biochemistry 40:15780–15788CrossRefPubMedGoogle Scholar
  43. Rakhimberdieva M, Stadnichuk I, Elanskaya I, Karapetyan N (2004) Carotenoid-induced quenching of the phycobilisome fluorescence in photosystem II-deficient mutant of Synechocystis sp. FEBS Lett 574:85–88CrossRefPubMedGoogle Scholar
  44. 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. Alliance Communication Group, Lawrence KS, pp 577–579Google Scholar
  45. Scott M, McCollum C, Vasil’ev S, Crozier C, Espie G, Krol M, Huner N, Bruce D (2006) Mechanism of the down regulation of photosynthesis by blue-light in a the cyanobactrium Synechocystis PCC 6803. Biochemistry 45:8952–8958CrossRefPubMedGoogle Scholar
  46. Siefermann-Harms D (1988) Fluorescence properties of isolated chlorophyll-protein complexes. In: Lichtenthaler HK (ed) Application of Chlorophyll Fluorescence. Kluwer Academic Publisher, Dordrecht, pp 45–54Google Scholar
  47. Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K, Murata N (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15:6416–6425PubMedGoogle Scholar
  48. Van Dorssen RJ, Plijte JJ, Decker J, den Ouden A, Amesz J, van Gorkom HJ (1987) Spectroscopic properties of chloroplast grana membranes and of the core of photosystem II. Biochim Biophys Acta 890:134–143CrossRefGoogle Scholar
  49. van Thor JJ, Mullineaux CW, Matthijs HC, Hellingwerf KJ (1998) Light harvesting and state transitions in cyanobacteria. Bot Acta 111:430–443Google Scholar
  50. Vernotte C, Picaud M, Kirilovsky D, Olive J, Ajlani G, Astier C (1992) Changes in the photosynthetic apparatus in the cyanobacterium Synechocystis sp PCC 6714 following light-to-dark and dark-to-light transitions. Photosynth Res 32:45–57CrossRefGoogle Scholar
  51. Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld C, Kirilovsky D (2005) The water-soluble orange carotenoid protein (OCP) involved in photoprotective mechanisms in Synechocystis PCC 6803. Paper presented at the IV Euroconference on the Molecular Bioenergetics of Cyanobacteria. San Feliu de Guixols, Spain, 21–26 May 2005Google Scholar
  52. Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld C, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007CrossRefPubMedGoogle Scholar
  53. Wilson A, Boulay C, Wilde A, Kerfeld C, Kirilovsky D (2007) Light induced energy dissipation in iron-starved cyanobacteria. Roles of OCP and IsiA proteins. Plant Cell 19:656–672CrossRefPubMedGoogle Scholar
  54. Wollman F-A (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20:3623–3630CrossRefPubMedGoogle Scholar
  55. Wu YP, Krogmann DW (1997) The orange carotenoid protein of Synechocystis PCC 6803. Biochim Biophys Acta 1322:1–7 CrossRefPubMedGoogle Scholar
  56. Yeremenko N, Kouril R, Ihalainem J, D’Haene S, van Oosterwijk N, Andrizhiyevkaya E, Keegstra W, Dekker H, Hagemann M, Boekema E, Matthijs H, Dekker J (2004) Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43:10308–10313CrossRefPubMedGoogle Scholar
  57. Yousef N, Pistorius EK, Michel K-P (2003) Comparative analysis of idiA and isiA transcription under iron starvation and oxidative stress in Synechococcus elongatus PCC 7942 wild-type and selected mutants. Arch Microbiol 180:471–483CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.CEA, SB2SM, iBiTecS, URA 2096CNRSGif sur YvetteFrance

Personalised recommendations