Biochemistry (Moscow)

, Volume 81, Issue 8, pp 858–870 | Cite as

Photosystem II activity of wild type Synechocystis PCC 6803 and its mutants with different plastoquinone pool redox states

  • O. V. VoloshinaEmail author
  • Y. V. BolychevtsevaEmail author
  • F. I. Kuzminov
  • M. Y. Gorbunov
  • I. V. Elanskaya
  • V. V. Fadeev


To assess the role of redox state of photosystem II (PSII) acceptor side electron carriers in PSII photochemical activity, we studied sub-millisecond fluorescence kinetics of the wild type Synechocystis PCC 6803 and its mutants with natural variability in the redox state of the plastoquinone (PQ) pool. In cyanobacteria, dark adaptation tends to reduce PQ pool and induce a shift of the cyanobacterial photosynthetic apparatus to State 2, whereas illumination oxidizes PQ pool, leading to State 1 (Mullineaux, C. W., and Holzwarth, A. R. (1990) FEBS Lett., 260, 245-248). We show here that dark-adapted Ox mutant with naturally reduced PQ is characterized by slower QA reoxidation and O2 evolution rates, as well as lower quantum yield of PSII primary photochemical reactions (Fv/Fm) as compared to the wild type and SDH–mutant, in which the PQ pool remains oxidized in the dark. These results indicate a large portion of photochemically inactive PSII reaction centers in the Ox mutant after dark adaptation. While light adaptation increases Fv/Fm in all tested strains, indicating PSII activation, by far the greatest increase in Fv/Fm and O2 evolution rates is observed in the Ox mutant. Continuous illumination of Ox mutant cells with low-intensity blue light, that accelerates QA reoxidation, also increases Fv/Fm and PSII functional absorption cross-section (590 nm); this effect is almost absent in the wild type and SDH–mutant. We believe that these changes are caused by the reorganization of the photosynthetic apparatus during transition from State 2 to State 1. We propose that two processes affect the PSII activity during changes of light conditions: 1) reversible inactivation of PSII, which is associated with the reduction of electron carriers on the PSII acceptor side in the dark, and 2) PSII activation under low light related to the increase in functional absorption cross-section at 590 nm.


cyanobacteria mutants photosystem II plastoquinone pool state transitions of photosynthetic apparatus 



2,5-dibromo-3-methyl-6-isopropyl-pbenzoquinone (dibromo-thymoquinone)


3-(3,4dichlorophenyl)-1,1'-dimethylurea (diuron)




ferredoxin-NADP oxidoreductase


a terminal oxidase-lacking mutant






photosystem 2 (1)

QA and QB

primary and secondary PSII quinone electron acceptors


a succinate dehydrogenase-lacking mutant


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  1. 1.
    Mullineaux, C. W., and Holzwarth, A. R. (1990) A proportion of photosystem IIcore complexes are decoupled from the phycobilisome in light-state 2 in the cyanobacterium Synechococcus 6301, FEBS Lett., 260, 245–248.CrossRefGoogle Scholar
  2. 2.
    Bonaventura, C., and Myers, J. (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa, Biochim. Biophys. Acta, 189, 366–383.CrossRefPubMedGoogle Scholar
  3. 3.
    Murata, N. (1969) Control of excitation transfer in photosynthesis: I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum, Biochim. Biophys. Acta, 172, 242–251.CrossRefPubMedGoogle Scholar
  4. 4.
    Fork, D. C., and Satoh, K. (1983) State I–state II transitions in the thermophilic blue-green alga (cyanobacterium) Synechococcus lividus, Photochem. Photobiol., 37, 421–427.CrossRefGoogle Scholar
  5. 5.
    Allen, J. F. (2003) State transitions–a question of balance, Science, 299, 1530–1532.CrossRefPubMedGoogle Scholar
  6. 6.
    Mullineaux, C. W., and Allen, J. F. (1990) State 1–state 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between photosystems I and II, Photosynth. Res., 23, 297–311.CrossRefPubMedGoogle Scholar
  7. 7.
    Mao, H.-B., Li, G.-F., Ruan, X., Wu, Q.-Yu, Gong, Y.-D., Zhang, X.-F., and Zhao, N.-M. (2002) The redox state of plastoquinone pool regulates state transitions via cytochrome b 6/f complex in Synechocystis sp. PCC 6803, FEBS Lett., 519, 82–86.CrossRefPubMedGoogle Scholar
  8. 8.
    Mullineaux, C. W., and Allen, J. F. (1988) Fluorescence induction transients indicate dissociation of photosystem IIfrom the phycobilisome during the state 2 transition in the cyanobacterium Synechococcus 6301, Biochim. Biophys. Acta, 934, 96–107.CrossRefGoogle Scholar
  9. 9.
    Rakhimberdieva, M. G., Boichenko, V. A., Karapetyan, N. V., and Stadnichuk, I. N. (2001) Interaction of phycobilisomes with photosystem IIdimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis, Biochemistry, 40, 15780–15788.CrossRefPubMedGoogle Scholar
  10. 10.
    Mullineaux, C. W., and Allen, J. F. (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.CrossRefGoogle Scholar
  11. 11.
    Huang, Ch., Yuan, X., Zhao, J., and Bryant, D. A. (2003) Kinetic analyses of state transitions of the cyanobacterium Synechococcus sp. PCC 7002 and its mutant strains impaired in electron transport, Biochim. Biophys. Acta, 1607, 121–130.CrossRefPubMedGoogle Scholar
  12. 12.
    Mi, H., Endo, T., Schreiber, U., Ogawa, T., and Asada, K. (1992) Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis sp. PCC 6803, Plant Cell Physiol., 33, 1233–1237.Google Scholar
  13. 13.
    Howitt, C. A., Smith, G. D., and Day, D. A. (1993) Cyanide-insensitive oxygen uptake and pyridine nucleotide dehydrogenases in the cyanobacterium Anabaena PCC 7120, Biochim. Biophys. Acta, 1141, 313–320.CrossRefGoogle Scholar
  14. 14.
    Cooley, J. W., Howitt, C. A., and Vermaas, W. F. J. (2000) Succinate:quinol oxidoreductase in the cyanobacterium Synechocystis sp. strain PCC 6803: presence and function in metabolism and electron transport, J. Bacteriol., 182, 714–722.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Pils, D., and Schmetterer, G. (2001) Characterization of three bioenergetically active respiratory terminal oxidases in the cyanobacterium Synechocystis sp. strain PCC 6803, FEMS Lett., 203, 217–222.CrossRefGoogle Scholar
  16. 16.
    Meunier, P. C., Colon-Lopez, M. S., and Sherman, L. A. (1997) Temporal changes in state transitions and photosystem organization in the unicellular, diazotrophic cyanobacterium Cyanothece sp. ATCC 51 142, Plant Physiol., 115, 991–1000.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Kirilovsky, D. (2014) Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions, Photosynth. Res., 126, 3–17.CrossRefPubMedGoogle Scholar
  18. 18.
    Mullineaux, C. W., Tobin, M. J., and Jones, G. R. (1997) Mobility of photosynthetic complexes in thylakoid membranes, Nature, 390, 421–424.CrossRefGoogle Scholar
  19. 19.
    Schluchter, W. M., Shen, G., Zhao, J., and Bryant, D. A. (1996) Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC 7002: a new model for state transitions in cyanobacteria, Photochem. Photobiol., 64, 53–66.CrossRefPubMedGoogle Scholar
  20. 20.
    Ivanov, A. G., Krol, M., Sveshnikov, D., Selstam, E., Sandstrom, St., Koochek, M., Park, Y.-I., Vasil’ev, S., Bruce, D., Oquist, G., and Huner, N. P. A. (2006) Iron deficiency in cyanobacteria causes monomerization of photosystem I trimers and reduces the capacity for state transitions and the effective absorption cross section of photosystem I in vivo, Plant Physiol., 141, 1436–1445.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Zhang, R., Xie, J., and Zhao, J. (2009) The mobility of PSI and PQmolecules in Spirulina platensis cells during state transition, Photosynth. Res., 99, 107–113.CrossRefPubMedGoogle Scholar
  22. 22.
    McConnell, M. D., Koop, R., Vasil’ev, S., and 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.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Cooley, J. W., and Vermaas, W. F. J. (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological function, J. Bacteriol., 183, 4251–4258.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Howitt, C. A., Cooley, J. W., Wiskich, J. T., and Vermaas, W. F. J. (2001) A strain of Synechocystis sp. PCC 6803 without photosynthetic oxygen evolution and respiratory oxygen consumption: implications for the study of cyclic photosynthetic electron transport, Planta, 214, 46–56.CrossRefPubMedGoogle Scholar
  25. 25.
    Ma, W., Mi, H., and Shen, Yu. (2010) Influence of the redox state of QA on phycobilisome mobility in the cyanobacterium Synechocystis sp. strain PCC6803, J. Luminesc., 130, 1169–1173.CrossRefGoogle Scholar
  26. 26.
    Campbell, D., Hurry, V., Clarke, A. K., Gustafsson, P., and Oquist, G. (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation, Microbiol. Mol. Biol. Rev., 62, 667–683.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Howitt, C. A., and Vermaas, W. F. J. (1998) Quinol and cytochrome oxidases in the cyanobacterium Synechocystis PCC 6803, Biochemistry, 37, 17944–17951.CrossRefPubMedGoogle Scholar
  28. 28.
    Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., and Stanier, R. Y. (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria, J. Gen. Microbiol., 111, 1–61.Google Scholar
  29. 29.
    Lichtenthaler, H. K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes, Methods Enzymol., 148C, 350–382.CrossRefGoogle Scholar
  30. 30.
    Schreiber, U., Schliwa, U., and Bilger, W. (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer, Photosynth. Res., 10, 51–62.CrossRefPubMedGoogle Scholar
  31. 31.
    Berry, S., Schneider, D., Vermaas, W. F. J., and Roegner, V. (2002) Electron transport routes in whole cells of Synechocystis sp. strain PCC 6803: the role of the cytochrome bd-type oxidase, Biochemistry, 41, 3422–3429.CrossRefPubMedGoogle Scholar
  32. 32.
    Gorbunov, M. Y., and Falkowski, P. G. (2005) in Photosynthesis. Fundamental Aspects to Global Perspectives: 13th Int. Congr. on Photosynthesis (Van der Est, A., and Bruce, D., eds.) Alliance Communication Group, Lawrence, Kansas, pp. 1029–1031.Google Scholar
  33. 33.
    Kolber, Z. S., Prasil, O., and Falkowski, P. G. (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols, Biochim. Biophys. Acta, 1367, 88–106.CrossRefPubMedGoogle Scholar
  34. 34.
    Joliot, A., and Joliot, P. (1964) Kinetic study of the potochemical reaction liberating oxygen during photosynthesis, CR Hebd. Seances Acad. Sci., 258, 4622–4625.Google Scholar
  35. 35.
    Lavergne, J., and Trissl, Y. W. (1995) Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units, Biophys. J., 68, 2474–2492.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Bolychevtseva, Y. V., Kuzminov, F. I., Elanskaya, I. V., Gorbunov, M. Y., and Karapetyan, N. V. (2015) Photosystem activity and state transitions of the photosynthetic apparatus in cyanobacterium Synechocystis PCC 6803 mutants with different redox state of the plastoquinone pool, Biochemistry (Moscow), 80, 50–60.CrossRefGoogle Scholar
  37. 37.
    Zhu, X.-G., Govindjee, Baker, N. R., D’Sturler, E., Ort, D. R., and Long, S. P. (2005) Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with photosystem II, Planta, 223, 114–133.CrossRefPubMedGoogle Scholar
  38. 38.
    Talts, E., Oja, V., Ramma, H., Rasulov, B., Anijalg, A., and Laisk, A. (2007) Dark inactivation of ferredoxin-NADP reductase and cyclic electron flow under far-red light in sunflower leaves, Photosynth. Res., 94, 109–120.CrossRefPubMedGoogle Scholar
  39. 39.
    Pschorn, R., Ruhle, W., and Wild, A. (1988) Structure and function of ferredoxin-NADP+-oxidoreductase, Photosynth. Res., 17, 217–229.CrossRefPubMedGoogle Scholar
  40. 40.
    Pelroy, R. A., and Bassham, J. A. (1972) Photosynthetic and dark carbon metabolism in unicellular blue-green algae, Arch. Microbiol., 86, 25–38.Google Scholar
  41. 41.
    Pelroy, R. A., Levine, G. A., and Bassham, J. A. (1976) Kinetics of light-dark CO2 fixation and glucose assimilation by Aphanocapsa 6714, J. Bacteriol., 128, 633–643.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Keren, N., Berg, A., Van Kan, P. J. M., Levanon, H., and Ohad, I. (1997) Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: the role of back electron flow, Proc. Natl. Acad. Sci. USA, 94, 1579–1584.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Ohad, I., Berg, A., Berkowicz, S. M., Kaplan, A., and Keren, N. (2011) Photoinactivation of photosystem II: is there more than one way to skin a cat? Physiol. Plant., 142, 79–86.CrossRefPubMedGoogle Scholar
  44. 44.
    Van Wijk, K. J., and Van Hasselt, Ph. R. (1993) Photoinhibition of photosystem II in vivo is preceded by down-regulation through light-induced acidification of the lumen: consequences for the mechanism of photoinhibition in vivo, Planta, 189, 359–368.CrossRefPubMedGoogle Scholar
  45. 45.
    Leitsch, J., Schnettger, B., Critchley, Ch., and Krause, G. H. (1994) Two mechanisms of recovery from photoinhibition in vivo: reactivation of photosystem II related and unrelated to D1-protein turnover, Planta, 194, 15–21.CrossRefGoogle Scholar
  46. 46.
    Ivanov, A. G., Sane, P. V., Hurry, V., Oquist, G., and Huner, N. P. A. (2008) Photosystem II reaction centre quenching: mechanisms and physiological role, Photosynth. Res., 98, 565–574.CrossRefPubMedGoogle Scholar
  47. 47.
    Andersson, B., and Barber, J. (1996) in Photosynthesis and the Environment. Advances in Photosynthesis and Respiration (Baker, N. R., ed.) Kluwer Academic Publishers, Springer, Dordrecht, Vol. 5, pp. 101–121.CrossRefGoogle Scholar
  48. 48.
    Horton, P., Ruban, A. V., and Walters, R. G. (1994) Regulation of light harvesting in green plants, Plant Physiol., 106, 415–420.PubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • O. V. Voloshina
    • 1
    Email author
  • Y. V. Bolychevtseva
    • 2
    Email author
  • F. I. Kuzminov
    • 1
    • 3
  • M. Y. Gorbunov
    • 3
  • I. V. Elanskaya
    • 4
  • V. V. Fadeev
    • 1
  1. 1.International Laser CenterLomonosov Moscow State UniversityMoscowRussia
  2. 2.Bach Institute of Biochemistry, Research Center of BiotechnologyRussian Academy of SciencesMoscowRussia
  3. 3.Department of Marine and Coastal SciencesRutgers, The State University of New JerseyNew BrunswickUSA
  4. 4.Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia

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