Abstract
Cyanobacteria are photosynthetic prokaryotes and widely used for photosynthetic research as model organisms. Partly due to their prokaryotic nature, however, estimation of photosynthesis by chlorophyll fluorescence measurements is sometimes problematic in cyanobacteria. For example, plastoquinone pool is reduced in the dark-acclimated samples in many cyanobacterial species so that conventional protocol developed for land plants cannot be directly applied for cyanobacteria. Even for the estimation of the simplest chlorophyll fluorescence parameter, F v/F m, some additional protocol such as addition of DCMU or illumination of weak blue light is necessary. In this review, those problems in the measurements of chlorophyll fluorescence in cyanobacteria are introduced, and solutions to those problems are given.
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Abbreviations
- DCMU:
-
3-(3, 4-Dichlorophenyl)-1, 1-dimethylurea
- F m :
-
Maximum fluorescence determined under oxidized plastoquinone pool conditions
- F m′ :
-
Maximum fluorescence under reduced plastoquinone pool conditions
- F 0 :
-
Minimum fluorescence under oxidized plastoquinone pool conditions
- F 0′ :
-
Minimum fluorescence under reduced plastoquinone pool conditions
- F s :
-
Stable fluorescence level
- F v/F m :
-
Chlorophyll fluorescence parameter indicating the maximum quantum yield of Photosystem II calculated as (F m − F 0)/F m
- NDH:
-
NAD(P)H dehydrogenase
- OCP:
-
Orange carotenoid protein
- PFD:
-
Photon flux density
- PQ:
-
Plastoquinone
- PS:
-
Photosystem
References
Acuña AM, Snellenburg JJ, Gwizdala M, Kirilovsky D, van Grondelle R, van Stokkum IHM (2016) Resolving contribution of the uncoupled phycobilisomes to cyanobacterial pulse-amplitude modulated (PAM) fluorometry signals. Photosynth Res 127:91–102
Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro E-M (2013) Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. PNAS 110:4111–4116
Allen MM, Smith AJ (1969) Nitrogen chlorosis in blue-green algae. Arch Microbiol 69:114–120
Aoki M, Katoh S (1982) Oxidation and reduction of plastoquinone by photosynthetic and respiratory electron transport in cyanobacterium Synechococcus sp. Biochim Biophys Acta 682:307–314
Bailey S, Mann NH, Robinson C, Scanlan DJ (2005) The occurrence of rapidly reversible non-photochemical quenching of chlorophyll a fluorescence in cyanobacteria. FEBS Lett 579:275–280
Bailey S, Melis A, Mackey KRM, Cardol P, Finazzi G, van Dijken G, Berg GM, Arrigo K, Shrager J, Grossman A (2008) Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim Biophys Acta 1777:269–276
Battchikova N, Eisenhut M, Aro EM (2011) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 1807:935–944
Blot N, Wu X-J, Thomas J-C, Zhang J, Garczarek L, Böhm S, Tu J-M, Zhou M, Plöscher M, Eichacker L, Partensky F, Scheer H, Zhao K-H (2009) Phycourobilin in trichromatic phycocyanin from oceanic cyanobacteria is formed post-translationally by a phycoerythrobilin lyase-isomerase. J Biol Chem 284:9290–2928
Campbell D, Öquist G (1996) Predicting light acclimation in cyanobacteria from nonphotochemical quenching of photosystem II fluorescence, which reflects state transitions in these organisms. Plant Physiol 111:1293–1298
Campbell D, Hurry V, Clarke AK, Gustafsson P, Öquist G (1998) Chlorophyll fluorescence analysis of cyanobacterial photosynthesis and acclimation. Microbiol Mol Biol Rev 62:667–683
Cooley JW, Vermaas WFJ (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
de Vitry C, Ouyang Y, Finazzi G, Wollman F-A, Kallas T (2004) The chloroplast Rieske iron-sulfur protein at the crossroad of electron transport and signal transduction. J Biol Chem 279:44621–44627
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 125:1988–2000
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 1457:229–242
Ermakova M, Huokko T, Richaud P, Bersanini L, Howe CJ, Lea-Smith DJ, Peltier G, Allahverdiyeva Y (2016) Distinguishing the roles of thylakoid respiratory terminal oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 171:1307–1319
Fujita Y (1997) A study on the dynamic features of photosystem stoichiometry: accomplishments and problems for future studies. Photosynth Res 53:83–93
Genty B, Wonders J, Baker NR (1990) Non-photochemical quenching of Fo in leaves is emission wavelength dependent: consequences for quenching analysis and its interpretation. Photosynth Res 26:133–139
Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160
Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749
Hayashi R, Shimakawa G, Shaku K, Shimizu S, Akimoto S, Yamamoto H, Amako K, Sugimoto T, Tamoi M, Makino A and Miyake C (2014) O2-dependent large electron flow functioned as an electron sink, replacing the steady-state electron flux in photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803, but not in the cyanobacterium Synechococcus sp. PCC 7942. Biosci Biotech Biochem 78:384–393
Kaňa R, Kotabová E, Komárek O, Šedivá B, Papageorgiou GC, Prášil O (2012). The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta 1817:1237–1247
Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7–16
Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105–115
Krause GH, Weis E (1984) Chlorophyll fluorescence as a tool in plant physiology. II. Interpretation of fluorescence signals. Photosynth Res 5:139–157
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349
Kühl M, Chen M, Ralph PJ, Schreiber U, Larkum AW (2005) Ecology: a niche for cyanobacteria containing chlorophyll d. Nature 433:820–820
Lea-Smith DJ, Ross N, Zori M, Bendall DS, Dennis JS, Scott SA, Smith AG, Howe CJ (2013) Thylakoid terminal oxidase are essential for the cyanobacterium Synechocystis sp. PCC 6803 to survive rapidly changing light intensities. Plant Physiol 162:484–495
Li H, Sherman LA (2002) Characterization of Synechocystis sp. strain PCC 6803 and ∆nbl mutants under nitrogen-deficient conditions. Arch Microbiol 178:256–266
Mimuro M, Kikuchi H (2003) Antenna systems and energy transfer in cyanophyta and rhodophyta. In: Green BR, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer, Dordrecht, pp 281–306
Misumi M, Katoh H, Tomo T, Sonoike K (2016) Relationship between photochemical quenching and non-photochemical quenching in six species of cyanobacteria reveals species difference in redox state and species commonality in energy dissipation. Plant Cell Physiol 57:1510–1517
Mullineaux CW, 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 205:155–160
Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393
Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390:421–424
Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron floe around photosystem I is essential for photosynthesis. Nature 429:579–582
Ogawa T, Sonoike K (2015) Dissection of respiration and photosynthesis in the cyanobacterium Synechocystis sp. PCC 6803 by the analysis of chlorophyll fluorescence. J Photochem Photobiol B 144:61–67
Ogawa T, Sonoike K (2016) Effects of bleaching by nitrogen deficiency on the quantum yield of photosystem II in Synechocystis sp. PCC 6803 revealed by chlorophyll fluorescence measurement. Plant Cell Physiol 57:558–567
Ogawa T, Harada T, Ozaki H, Sonoike K (2013) Disruption of the ndhF1 gene affects chlorophyll fluorescence through state transition in the cyanobacterium Synechocystis sp. PCC 6803, resulting in apparent high efficiency of photosynthesis. Plant Cell Physiol 54:1164–1171
Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components-calculation of qP and Fv′/Fm′ without measuring Fo′. Photosynth Res 54:135–142
Ozaki H, Sonoike K (2009) Quantitative analysis of the relationship between induction kinetics of chlorophyll fluorescence and function of genes in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 101:47–58
Ozaki H, Ikeuchi M, Ogawa T, Fukuzawa H, Sonoike K (2007) Large scale analysis of chlorophyll fluorescence kinetics in Synechocystis sp. PCC 6803: identification of the factors involved in the modulation of photosystem stoichiometry. Plant Cell Physiol 48:451–458
Peschek GA, Schmetterer G (1982) Evidence for plastoquinol-cytochrome f/b 563 reductase as a common electron donor to P700 and cytochrome oxidase in cyanobacteria. Biochim Biophys Res Commun 108:1188–1195
Pfündel E (1998) Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56:185–195
Pfündel EE, Klughammer C, Meister A, Cerovic ZG (2013) Deriving fluorometer-specific values of relative PSI fluorescence intensity from quenching of F(0) fluorescence in leaves of Arabidopsis thaliana and Zea mays. Photosynth Res 114:189–206
Quick WP, Stitt M (1989) An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves. Biochim Biophys Acta 977:287–296
Schreiber U, Schliwa U, 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
Schreiber U, Endo T, Mi H, Asada K (1995) Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol 36:873–882
Schuurmans RM, van Alphen P, Schuurmans JM, Matthijs HCP, Hellingwerf KJ (2015) Comparison of the photosynthetic yield of cyanobacteria and green algae: different methods give different answers. PLoS ONE 10:e0139061
Shimakawa G, Shaku K, Nishi A, Hayashi R, Yamamoto H, Sakamoto K, Makino A, Miyake C (2015) FLAVODIIRON2 and FLAVODIIRON4 proteins mediate an oxygen-dependent alternative electron flow in Synechocystis sp. PCC 6803 under CO2-limited conditions. Plant Physiol 167:472–480
Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64
Sonoike K, Hihara Y, Ikeuchi M (2001) Physiological significance of the regulation of photosystem stoichiometry upon high light acclimation of Synechocystis sp. PCC 6803. Plant Cell Physiol 42:379–384
Zhang P, Allahverdiyeva Y, Eisenhut M, Aro EM (2009) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS ONE 4:e5331
Acknowledgements
This work was supported by JSPS Grant-in-Aid for Scientific Research on Innovative Areas (No. 16H06552 and No. 16H06553 to K.S.) and Grant-in-Aid for Scientific Research (B) (No. 16H04809 to K.S.), as well as by Grant-in-Aid for JSPS Research Fellow (No. 26-7221 to T.O.). We thank Dr. Yukako Hihara for the critical reading of the manuscript.
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Takako Ogawa and Masahiro Misumi have contributed equally to this work.
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Ogawa, T., Misumi, M. & Sonoike, K. Estimation of photosynthesis in cyanobacteria by pulse-amplitude modulation chlorophyll fluorescence: problems and solutions. Photosynth Res 133, 63–73 (2017). https://doi.org/10.1007/s11120-017-0367-x
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DOI: https://doi.org/10.1007/s11120-017-0367-x