Abstract
To better understand how photosystem (PS) activity is regulated during state transitions in cyanobacteria, we studied photosynthetic parameters of photosystem II (PSII) and photosystem I (PSI) in Synechocystis PCC 6803 wild type (WT) and its mutants deficient in oxidases (Ox−) or succinate dehydrogenase (SDH−). Dark-adapted Ox− mutant, lacking the oxidation agents, is expected to have a reduced PQ pool, while in SDH− mutant the PQ pool after dark adaptation will be more oxidized due to partial inhibition of the respiratory chain electron carriers. In this work, we tested the hypothesis that control of balance between linear and cyclic electron transport by the redox state of the PQ pool will affect PSII photosynthetic activity during state transition. We found that the PQ pool was reduced in Ox− mutant, but oxidized in SDH− mutant after prolonged dark adaptation, indicating different states of the photosynthetic apparatus in these mutants. Analysis of variable fluorescence and 77K fluorescence spectra revealed that the WT and SDH− mutant were in State 1 after dark adaptation, while the Ox− mutant was in State 2. State 2 was characterized by ∼1.5 time lower photochemical activity of PSII, as well as high rate of P700 reduction and the low level of P700 oxidation, indicating high activity of cyclic electron transfer around PSI. Illumination with continuous light 1 (440 nm) along with flashes of light 2 (620 nm) allowed oxidation of the PQ pool in the Ox− mutant, thus promoting it to State 1, but it did not affect PSII activity in dark adapted WT and SDH− mutant. State 1 in the Ox− mutant was characterized by high variable fluorescence and P700+ levels typical for WT and the SDH− mutant, indicating acceleration of linear electron transport. Thus, we show that PSII of cyanobacteria has a higher photosynthetic activity in State 1, while it is partially inactivated in State 2. This process is controlled by the redox state of PQ in cyanobacteria through enhancement/inhibition of electron transport on the acceptor side of PSII.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- CtaI, CtaII, and Cyd:
-
terminal oxidases
- cyt b 6 /f :
-
complex of b 6 /f cytochromes
- DCMU:
-
dichlorophenyl-dimethyl urea
- Fd:
-
ferredoxin
- FNR:
-
ferredoxin:NADP-oxidoreductase
- NAD(P+)/NAD(P)H:
-
oxidized/reduced nicotine amide adenine dinucleotide (phosphate)
- Ox− :
-
mutant deficient in terminal oxidases
- PBS:
-
phycobilisome
- PQ:
-
plastoquinone
- PSII(I):
-
photosystem II(I)
- QA/QA − and QB/QB − :
-
primary and secondary quinone electron acceptors of PSII in oxidized/reduced states
- SDH− :
-
mutant deficient in succinate dehydrogenase (succinate:quinol oxidoreductase)
- WT:
-
wild type
References
Horton, P., Ruban, A. V., and Walters, R. G. (1996) Regulation of light harvesting in green plants, Ann. Rev. Plant Physiol. Plant Mol. Biol., 47, 655–684.
Karapetyan N. V. (2007) Non-photochemical quenching of fluorescence in cyanobacteria, Biochemistry (Moscow), 72, 1127–1135.
Bonaventura, C., and Myers, J. (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa, Biochim. Biophys. Acta, 189, 366–383.
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.
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.
Allen J. F. (2003) State transitions—a question of balance, Science, 299, 1530–1532.
Allen J. F., Bennett J., Steinback K. E., and Arntzen C. J. (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems, Nature, 291, 25–29.
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.
Allen, J. F. (1992) Protein phosphorylation in regulation of photosynthesis, Biochim. Biophys. Acta, 1098, 275–335.
Tsinoremas, N. F., Hubbard, J. A. M., Evens, M. C. W., and Allen, J. F. (1989) P700 photooxidation in state 1 and state 2 in cyanobacteria upon flash illumination with phycobilin- and chlorophyll-absorbed light, FEBS Lett., 256, 106–110.
Mullineaux, C. W. (1992) Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium, Biochim. Biophys. Acta, 1100, 285–292.
Rakhimberdieva M. G., Boichenko V. A., Karapetyan N. V., and Stadnichuk I. N. (2001) Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis, Biochemistry, 40, 15780–15788.
Melis, A., Mullineaux, C. W., and Allen, J. F. (1989) Acclimation of the photosynthetic apparatus to photosystem I or photosystem II light: evidence from quantum yield measurements and fluorescence spectroscopy of cyanobacterial cells, Z. Naturforsch., 44c, 109–118.
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.
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.
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.
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.
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.
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 b6 f complex in Synechocystis sp. PCC 6803, FEBS Lett., 519, 82–86.
Mullineaux, C. W., and Holzwarth, A. R. (1990) A proportion of photosystem II core complexes are decoupled from the phycobilisome in light-state 2 in the cyanobacterium Synechococcus 6301, FEBS Lett., 260, 245–248.
Mullineaux C. W., Tobin M. J., and Jones G. R. (1997) Mobility of photosynthetic complexes in thylakoid membranes, Nature, 390, 421–424.
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.
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 51142, Plant Physiol., 115, 991–1000.
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.
Zhang, R., and Zhao, J. X. J. (2009) The mobility of PSI and PQ molecules in Spirulina platensis cells during state transition, Photosynth. Res., 99, 107–113.
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.
Huang, Ch., Yuan, X., Zhao, J., and Bryant, D. A. (2003) Kinetics 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.
Mi, H., Klughammer, Ch., and Schreiber, U. (2000) Light-induced dynamic changes of NADPH fluorescence in Synechocystis PCC 6803 and its ndhB-defective mutant M55, Plant Cell Physiol., 41, 1129–1135.
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.
Van Thor, J. J., Jeanjean, R., Havaux, M., Sjollema, K. A., Joset, F., Hellingwerf, K. J., and Matthijs, H. C. P. (2000) Salt shock-inducible photosystem I cyclic electron transfer in Synechocystis PCC6803 relies on binding of ferredoxin:NADP+ reductase to the thylakoid membranes via its CpcD phycobilisome-linker homologous N-terminal domain, Biochim. Biophys. Acta, 1457, 129–144.
Thomas, D. J., Thomas, J., Youderian, Ph. A., and Herbert, St. H. (2001) Photoinhibition and light-induced cyclic electron transport in ndh − and psa0 − mutants of Synechocystis sp. PCC 6803, Plant Cell Physiol., 42, 803–812.
Finazzi, G., Rappaport, F., Furia, A., Fleischmann, M., Rochaix, J.-D., Zito, F., and Forti, G. (2002) Involvement of state transition in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii, EMBO Rep., 3, 280–285.
Barbagallo, R. P., Bergo, E., Barbato, R., and Forti, G. (2001) Photoinhibition of Chlamydomonas reinhardtii in state 1 and state 2, J. Biol. Chem., 276, 22251–22257.
Bolychevtseva, Y., Elanskaya, I. V., and Karapetyan, N. V. (2011) Regulation of cyclic electron transport through photosystem I in the mutant cells of the cyanobacterium Synechocystis sp. PCC 6803 devoid of respiratory dehydrogenases, Biochemistry (Moscow), 76, 427–437.
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.
Howitt C. A., and Vermaas W. F. J. (1998) Quinol and cytochrome oxidases in the cyanobacterium Synechocystis PCC 6803, Biochemistry, 37, 17944–17951.
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.
Lichtenthaler, H. K. (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes, in Methods in Enzymology, Vol. 148 (Colowick, S. P., and Kaplan, N. O., eds.) Academic Press Inc., San Diego, pp. 350–382.
Schreiber, U., Schliwa, U., and Bilger, W. (1986) Continuous recording of photochemical and non-photo-chemical chlorophyll fluorescence quenching with a new type of modulation fluorometer, Photosynth. Res., 10, 51–62.
Schreiber, U., Klughammer, C., and Neubauer, C. (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system, Z. Naturforsch., 43c, 686–698.
Mullineaux, C. W., and Allen, J. F. (1988) Fluorescence induction transients indicate dissociation of photosystem II from the phycobilisome during the State-2 transition in the cyanobacterium Synechococcus 6301, Biochim. Biophys. Acta, 934, 96–107.
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.
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.
Toth, S. Z., Schansker, G., and Strasser, R. J. (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient, Photosynth. Res., 93, 193–203.
Tsimilli-Michael, M., Stamatakis, K., and Papageorgiou, G. C. (2009) Dark-to-light transition in Synechococcus sp. PCC 7942 cells studied by fluorescence kinetics assesses plastoquinone redox poise in the dark and photosystem II fluorescence component and dynamics during state 2 to state 1 transition, Photosynth. Res., 99, 243–255.
Schansker, G., Toth, S. Z., and Strasser, R. J. (2006) Dark recovery of the Chl a fluorescence transient (OJIP) after light adaptation: the qT-component of non-photochemical quenching is related to an activated photosystem I acceptor side, Biochim. Biophys. Acta, 1757, 787–797.
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.
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.
Vass, I., and Cser, K. (2009) Janus-faced charge recombinations in photosystem II photoinhibition, Trends Plant Sci., 14, 200–205.
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.
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.
Demmig B., and Bjorkman O. (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77K) and photon yield of O2 evolution in the leaves of higher plants, Planta, 171, 171–184.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Published in Russian in Biokhimiya, 2015, Vol. 80, No. 1, pp. 65–78.
Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM14-182, January 4, 2015.
Rights and permissions
About this article
Cite this article
Bolychevtseva, Y.V., Kuzminov, F.I., Elanskaya, I.V. et al. 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 (2015). https://doi.org/10.1134/S000629791501006X
Received:
Revised:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S000629791501006X