Photosynthesis Research

, Volume 99, Issue 3, pp 227–241 | Cite as

Fluorescence changes accompanying short-term light adaptations in photosystem I and photosystem II of the cyanobacterium Synechocystis sp. PCC 6803 and phycobiliprotein-impaired mutants: State 1/State 2 transitions and carotenoid-induced quenching of phycobilisomes

  • Igor N. Stadnichuk
  • Evgeny P. Lukashev
  • Irina V. Elanskaya
Regular Paper


The features of the two types of short-term light-adaptations of photosynthetic apparatus, State 1/State 2 transitions, and non-photochemical fluorescence quenching of phycobilisomes (PBS) by orange carotene-protein (OCP) were compared in the cyanobacterium Synechocystis sp. PCC 6803 wild type, CK pigment mutant lacking phycocyanin, and PAL mutant totally devoid of phycobiliproteins. The permanent presence of PBS-specific peaks in the in situ action spectra of photosystem I (PSI) and photosystem II (PSII), as well as in the 77 K fluorescence excitation spectra for chlorophyll emission at 690 nm (PSII) and 725 nm (PSI) showed that PBS are constitutive antenna complexes of both photosystems. The mutant strains compensated the lack of phycobiliproteins by higher PSII content and by intensification of photosynthetic linear electron transfer. The detectable changes of energy migration from PBS to the PSI and PSII in the Synechocystis wild type and the CK mutant in State 1 and State 2 according to the fluorescence excitation spectra measurements were not registered. The constant level of fluorescence emission of PSI during State 1/State 2 transitions and simultaneous increase of chlorophyll fluorescence emission of PSII in State 1 in Synechocystis PAL mutant allowed to propose that spillover is an unlikely mechanism of state transitions. Blue–green light absorbed by OCP diminished the rout of energy from PBS to PSI while energy migration from PBS to PSII was less influenced. Therefore, the main role of OCP-induced quenching of PBS is the limitation of PSI activity and cyclic electron transport under relatively high light conditions.


Cyanobacterium Fluorescence emission Fluorescence excitation Photosynthetic action spectra Photosystem I Photosystem II Phycobilisome(s) State transitions 





Orange carotene-protein


Photosystem I and II





This publication is dedicated to the memory of Dr. V. Boichenko. We thank Dr. G. Ajlani for the generous gift of CK and PAL mutants. This study was supported by the Russian Foundation for Basic Researches (projects 06-04-48658 and 06-04-49304).


  1. Abasova L, Boulay C, Vass I, Kirilovsky D (2007) Non-photochemical-quenching mechanisms in the cyanobacterium Thermosynechococcus. Photosynth Res 91:255–256Google Scholar
  2. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85:15–32. doi: 10.1007/s11120-004-2143-y PubMedCrossRefGoogle Scholar
  3. Ajlani G, Vernotte C (1998) Construction and characterization of phycobiliprotein-less mutant of Synechocystis sp. PCC 6803. Plant Mol Biol 37:577–580. doi: 10.1023/A:1005924730298 PubMedCrossRefGoogle Scholar
  4. Ajlani G, Vernotte C, DiMagno L, Haselkorn R (1995) Phycobilisome core mutants of Synechocystis PCC 6803. Biochim Biophys Acta 1231:189–196. doi: 10.1016/0005-2728(95)00086-X CrossRefGoogle Scholar
  5. Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335PubMedGoogle Scholar
  6. Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326. doi: 10.1016/S1360-1385(01)02010-6 PubMedCrossRefGoogle Scholar
  7. Allen JF, Holmes NG (1986) A general model for regulation of photosynthetic unit function by protein phosphorylation. FEBS Lett 202:175–181. doi: 10.1016/0014-5793(86)80682-2 CrossRefGoogle Scholar
  8. Allen JF, Bennet J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291:21–25. doi: 10.1038/291021a0 CrossRefGoogle Scholar
  9. Bald D, Kruip J, Roegner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth Res 49:103–118. doi: 10.1007/BF00117661 CrossRefGoogle Scholar
  10. Biggins J, Bruce D (1989) Regulation of excitation energy transfer in organisms containing phycobilins. Photosynth Res 20:1–34. doi: 10.1007/BF00028620 CrossRefGoogle Scholar
  11. Biggins J, Campbell CL, Bruce D (1984) Mechanism of the light state transition in photosynthesis. Analysis of phosphorylated polypeptides in the red alga, Porphyridium cruentum. Biochim Biophys Acta 767:138–144. doi: 10.1016/0005-2728(84)90088-4 CrossRefGoogle Scholar
  12. Boichenko VA (2004) Study of the organization of photosynthetic units by action spectra of functional activity. Biophysics (Oxf) 49:238–247Google Scholar
  13. Boichenko VA, Pinevich AV, Stadnichuk IN (2007) Association of chlorophyll a/b-binding Pcb proteins with photosystems I and II in Prochlorothrix hollandica. Biochim Biophys Acta 1767:801–806. doi: 10.1016/j.bbabio.2006.11.001 PubMedCrossRefGoogle Scholar
  14. Bonaventura P, Meyers J (1969) Fluorescence and oxygen evolution for Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383. doi: 10.1016/0005-2728(69)90168-6 PubMedCrossRefGoogle Scholar
  15. Bruce D, Salehian O (1992) Laser-induced optoacoustic calorimetry of cyanobacteria. The efficiency of primary photosynthetic process in state 1 and state 2. Biochim Biophys Acta 1100:242–250Google Scholar
  16. Bruce D, Brimble S, Bryant DA (1989) State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974:66–73. doi: 10.1016/S0005-2728(89)80166-5 PubMedCrossRefGoogle Scholar
  17. 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 892:267–274Google Scholar
  18. El Bissati K, Delphin E, Murata N, Etienne A-L, Kirilovsky D (2001) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis sp. PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457:229–242Google Scholar
  19. Emlyn-Jones D, Ashby MK, Mullineaux CW (1999) A gene required for the regulation of photosynthetic light-harvesting in the cyanobacterium Synechocystis 6803. Mol Microbiol 33:1050–1058. doi: 10.1046/j.1365-2958.1999.01547.x PubMedCrossRefGoogle Scholar
  20. Ferreira K, Iverson T, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838. doi: 10.1126/science.1093087 PubMedCrossRefGoogle Scholar
  21. Herdman M, Delaney SF, Carr NG (1973) A new medium for the isolation and growth of auxotrophic mutants of the blue–green alga, Anacystis nidulans. J Gen Microbiol 79:233–237Google Scholar
  22. Jordan P, Fromme P, Witt HT, Klukas W, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917. doi: 10.1038/35082000 PubMedCrossRefGoogle Scholar
  23. Joshua S, Mullineaux CW (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135:2112–2119. doi: 10.1104/pp.104.046110 PubMedCrossRefGoogle Scholar
  24. Kirilovsky D, Wilson A (2007) A new photoactive protein acting as a sensor of light intensity: the orange carotenoid protein (OCP). Photosynth Res 91:291–292Google Scholar
  25. Koblizek M, Komenda J, Masojdek J (1998) State transitions in the cyanobacterium Synechococcus PCC 7942. Mobile antenna or spillover? In: Garab G (ed) Photosynthesis: mechanisms and effects, vol I. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 213–216Google Scholar
  26. Kondo K, Ochiai Y, Katayama M, Ikeuchi M (2007) The membrane-associated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna. Plant Physiol 144:1200–1210. doi: 10.1104/pp.107.099267 PubMedCrossRefGoogle Scholar
  27. Ley AC, Butler WL (1980) Energy distribution in the photochemical apparatus of Porphyridium cruentum in state I and state II. Biochim Biophys Acta 592:349–363. doi: 10.1016/0005-2728(80)90195-4 PubMedCrossRefGoogle Scholar
  28. Mao H-B, Li G-F, Li D-H, Wu Q-Y, Gong Y-D, Zhang X-F, Zhao N-M (2003) Effect of glycerol and high temperatures on structure and function of phycobilisomes in Synechocystis sp. PCC 6803. FEBS Lett 553:68–72. doi: 10.1016/S0014-5793(03)00973-6 PubMedCrossRefGoogle Scholar
  29. McConnell MD, Koop R, Vasil’ev S, Bruce D (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light-state transition. Plant Physiol 130:1201–1212. doi: 10.1104/pp.009845 PubMedCrossRefGoogle Scholar
  30. Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium. Biochim Biophys Acta 1100:285–292Google Scholar
  31. Mullineaux CW (1999) The thylakoid membranes of cyanobacteria: structure, dynamics and function. Aust J Plant Physiol 26:671–677CrossRefGoogle Scholar
  32. Mullineaux CW, Allen J (1986) The state 2 transition in the cyanobacterium Synechococcus 6301 can be driven by respiratory electron flow into the plastoquinone pool. FEBS Lett 205:155–160. doi: 10.1016/0014-5793(86)80885-7 CrossRefGoogle Scholar
  33. Mullineaux CW, Allen JF (1988) Fluorescence induction transients indicate dissociation of Photosystem II from the phycobilisomes during the State-2 transition in the cyanobacterium Synechococcus 6301. Biochim Biophys Acta 934:96–107. doi: 10.1016/0005-2728(88)90124-7 CrossRefGoogle Scholar
  34. Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393. doi: 10.1093/jxb/eri064 PubMedCrossRefGoogle Scholar
  35. Murata N (1969) Control of excitation transfer in photosynthesis. Biochim Biophys Acta 172:242–251. doi: 10.1016/0005-2728(69)90067-X PubMedCrossRefGoogle Scholar
  36. Olive J, Ajlani G, Astier C, Recouvreur M, Vernotte C (1997) Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis 6803. Biochim Biophys Acta 1319:275–282. doi: 10.1016/S0005-2728(96)00168-5 CrossRefGoogle Scholar
  37. Piven I, Ajlani G, Sokolenko A (2005) Phycobilisome linker proteins are phosphorylated in Synechocystis sp. PCC 6803. J Biol Chem 280:21667–21672. doi: 10.1074/jbc.M412967200 PubMedCrossRefGoogle Scholar
  38. Rakhimberdieva MG, Boichenko VA, Karapetyan NV, Stadnichuk IN (2001) Interaction of phycobilisomes with Photosystem II dimers and Photosystem I monomers and trimers in the cyanobacterium Spirulina platensis. Biochemistry 40:15780–15788. doi: 10.1021/bi010009t PubMedCrossRefGoogle Scholar
  39. 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 574:85–88. doi: 10.1016/j.febslet.2004.07.087 PubMedCrossRefGoogle Scholar
  40. Sarcina M, Tobin MJ, Mullineaux CW (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942. J Biol Chem 276:46830–46834. doi: 10.1074/jbc.M107111200 PubMedCrossRefGoogle Scholar
  41. Schluchter WM, Shen G, Zhao J, Bryant DA (1996) Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC7002: a new model for state transitions in cyanobacteria. Photochem Photobiol 64:53–66. doi: 10.1111/j.1751-1097.1996.tb02421.x PubMedCrossRefGoogle Scholar
  42. Scott M, McCollum S, Vasil’ev S, Crozier GS, Espie M, Croll M, Huner NPA, Bruce D (2006) Mechanism of down regulation of photosynthesis by blue light in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 45:8952–8958. doi: 10.1021/bi060767p PubMedCrossRefGoogle Scholar
  43. Stadnichuk IN, Boichenko VA (2007) Distribution of antenna complexes between photosystems I and II in cyanobacteria, prochlorophytes, cryptophytes, and red algae. Photosynth Res 91:253–254Google Scholar
  44. Stadnichuk IN, Boichenko VA, Rakhimberdieva MG, Karapetyan NV, Elanskaya IV (2004) Functions of phycobilisomes in delivery of excitation energy to photosystem I and photosystem II and carotenoid-induced protection of phycobilisomes against photobleaching. Proceedings of the 13th International Congress on Photosynthesis: Electronic ViewGoogle Scholar
  45. Suter GW, Mazzola P, Wendler J, Holzwarth AR (1984) Fluorescence decay kinetics in phycobilisomes isolated from the blue–green alga Synechococcus 6301. Biochim Biophys Acta 766:269–276. doi: 10.1016/0005-2728(84)90241-X CrossRefGoogle Scholar
  46. van Thor JJ, Mullineaux CW, Matthijs HCP, Hellingwerf KJ (1998) Light harvesting and state transitions in cyanobacteria. Bot Acta 111:430–443Google Scholar
  47. Westermann M, Ernst A, Brass S, Boger P, Wehrmeyer W (1994) Ultrastructure of cell wall, photosynthetic apparatus of the phycobilisome-less Synechocystis sp. strain BO 8402 and phycobilisome-containing derivative strain BO 9201. Arch Microbiol 162:222–232Google Scholar
  48. Williams WP, Allen JF (1987) State1/State2 changes in higher plants and algae. Photosynth Res 13:19–45. doi: 10.1007/BF00032263 CrossRefGoogle Scholar
  49. Wilson A, Ajlani G, Verbavatz J-M, Vass I, Kerfeld C, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation. Plant Cell 18:992–1007. doi: 10.1105/tpc.105.040121 PubMedCrossRefGoogle Scholar
  50. Wolman F-A (1979) Ultrastructural comparison of Cyanidium caldarium wild type and III-c mutant lacking phycobilisomes. Plant Physiol 63:375–381. doi: 10.1104/pp.63.2.375 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Igor N. Stadnichuk
    • 1
  • Evgeny P. Lukashev
    • 2
  • Irina V. Elanskaya
    • 2
  1. 1.A.N. Bakh Institute of Biochemistry Russian Academy of SciencesMoscowRussia
  2. 2.Biological DepartmentMoscow Lomonosov State UniversityMoscowRussia

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