Summary
Photosystem II (PSII) is conserved in all oxygenic photosynthetic organisms and is important for its unique ability to use energy from light to split water, generate molecular oxygen in the Earth’s atmosphere and drive electrons into the photosynthetic electron transport chain by reducing the plastoquinone (PQ) pool in the thylakoid membrane. The focus of this chapter is on alternative electron-transfer pathways on the acceptor side of PSII. Upon close examination of the literature there is evidence of exogenous electron acceptors that are reduced directly by the primary PQ electron acceptor (QA), bypassing the canonical terminal PQ-reduction (QB) site. These herbicide-insensitive electron-acceptor molecules include but are not limited to ferricyanide, synthetic cobalt coordination complexes, and cytochrome c. We also discuss experimental treatments to PSII such as cation exchange and herbicide treatment that have been shown to alter the redox midpoint potential (Em) of QA and impact electron transfer from QA to QB. The results described in this chapter provide a platform for understanding how electrons generated in PSII by photochemical water oxidation can be extracted from the electron-acceptor side of PSII for energy applications.
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References
Alcantara K, Munge B, Pendon Z, et al. (2006) Thin film voltammetry of spinach photosystem II. Proton-gated electron transfer involving the Mn4 cluster. J Am Chem Soc 128:14930–14937. doi: 10.1021/ja0645537
Allakhverdiev SI, Tsuchiya T, Watabe K, et al. (2011) Redox potentials of primary electron acceptor quinone molecule QA- and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d. P Natl Acad Sci USA 108:8054–8058. doi: 10.1073/pnas.1100173108
Ashizawa R, Noguchi T (2014) Effects of hydrogen bonding interactions on the redox potential and molecular vibrations of plastoquinone as studied using density functional theory calculations. Phys Chem Chem Phys 16:11864–11876. doi: 10.1039/c3cp54742f
Badura A, Guschin D, Esper B, et al. (2008) Photo-Induced Electron Transfer Between Photosystem 2 via Cross-linked Redox Hydrogels. Electroanal 20:1043–1047. doi: 10.1002/elan.200804191
Barr R, Crane FL, Giaquinta RT (1975) Dichlorophenylurea-insensitive reduction of silicomolybdic acid by chloroplast Photosystem II. Plant Physiol 55:460–462. doi:10.1104/pp.55.3.460
Bendall DS, Hill R (1968) Haem-proteins in photosynthesis. Ann Rev Plant Phys 167–186.
BĂ¼chel KH (1972) Mechanisms of action and structure activity relations of herbicides that inhibit photosynthesis. Pestic Sci 3:89–110. doi: 10.1002/ps.2780030113
Buser CA, Thompson LK, Diner BA, Brudvig GW (1990) Electron-transfer reactions in manganese-depleted photosystem II. Biochemistry-US 29:8977–8985. doi: 10.1021/bi00490a014
Chernev P, Zaharieva I, Dau H, Haumann M (2011) Carboxylate shifts steer interquinone electron transfer in photosynthesis. J Biol Chem 286:5368–5374. doi: 10.1074/jbc.M110.202879
De Wael K, De Belder S, Van Vlierberghe S, et al. (2010) Electrochemical study of gelatin as a matrix for the immobilization of horse heart cytochrome c. Talanta 82:1980–1985. doi: 10.1016/j.talanta.2010.08.019
Endo K, Mizusawa N, Shen J-R, et al. (2015) Site-directed mutagenesis of amino acid residues of D1 protein interacting with phosphatidylglycerol affects the function of plastoquinone QB in photosystem II. Photosynth Res 126:385–397. doi: 10.1007/s11120-015-0150-9
Ferreira KN, Iverson TM, Maghlaoui K, et al. (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838. doi: 10.1126/science.1093087
Fufezan C, Gross CM, Sjodin M, et al. (2007) Influence of the Redox Potential of the Primary Quinone Electron Acceptor on Photoinhibition in Photosystem II. J of Biol Chem 282:12492–12502. doi: 10.1074/jbc.M610951200
Giaquinta RT, Dilley RA (1975) A partial reaction in photosystem II: reduction of silicomolybdate prior to the site of dichlorophenyldimethylurea inhibition. Biochim Biophys Acta 387:288–305. doi:10.1016/0005-2728(75)90111-5
Guskov A, Kern J, Gabdulkhakov A, et al. (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342. doi: 10.1038/nsmb.1559
Hasegawa K, Noguchi T (2012) Molecular interactions of the quinone electron acceptors QA, QB, and QC in photosystem II as studied by the fragment molecular orbital method. Photosynth Res 120:113–123. doi: 10.1007/s11120-012-9787-9
Hauska G (1977) Artificial Acceptors and Donors. In: Photosynthesis I. Springer Berlin/Heidelberg, pp 253–265
Hill R (1937) Oxygen Evolved by Isolated Chloroplasts. Nature 139:881–882. doi: 10.1038/139881a0
Hill R, Scarisbrick R (1940) Production of Oxygen by Illuminated Chloroplasts. Nature 146:61–62. doi: 10.1038/146061a0
Ishikita H, Knapp E-W (2005) Control of quinone redox potentials in photosystem II: Electron transfer and photoprotection. J Am Chem Soc 127:14714–14720. doi: 10.1021/ja052567r
Itoh S, Kozuki T, Nishida K, et al. (2012) Two functional sites of phosphatidylglycerol for regulation of reaction of plastoquinone QB in photosystem II. Biochim Biophys Acta 1817:287–297. doi: 10.1016/j.bbabio.2011.10.002
Iwai M, Katoh H, Katayama M, Ikeuchi M (2004) PSII-Tc protein plays an important role in dimerization of photosystem II. Plant Cell Physiol 45:1809–1816. doi: 10.1093/pcp/pch207
Izawa S (1980) Acceptors and donors for chloroplast electron transport. Method Enzymol 69:413–434.
Kaminskaya O, Shuvalov VA, Renger G (2007) Evidence for a novel quinone-binding site in the photosystem II (PS II) complex that regulates the redox potential of cytochrome b559. Biochemistry-US 46:1091–1105. doi: 10.1021/bi0613022
Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7Å resolution. Proc Natl Acad Sci U S A 100:98–103. doi: 10.1073/pnas.0135651100
Kansy M, Wilhelm C, Goss R (2014) Influence of thylakoid membrane lipids on the structure and function of the plant photosystem II core complex. Planta 240:781–796. doi: 10.1007/s00425-014-2130-2
Kato Y, Noguchi T (2014) Long-range interaction between the Mn4CaO5 cluster and the non-heme iron center in photosystem II as revealed by FTIR spectroelectrochemistry. Biochemistry-US 53:4914–4923. doi: 10.1021/bi500549b
Kato M, Cardona T, Rutherford AW, Reisner E (2012a) Photoelectrochemical Water Oxidation with Photosystem II Integrated in a Mesoporous Indium–Tin Oxide Electrode. J Am Chem Soc 134:8332–8335. doi: 10.1021/ja301488d
Kato Y, Shibamoto T, Yamamoto S, et al. (2012b) Influence of the PsbA1/PsbA3, Ca2+/Sr2+ and Cl−/Br− exchanges on the redox potential of the primary quinone QA in Photosystem II from Thermosynechococcus elongatus as revealed by spectroelectrochemistry. Biochim Biophys Acta 1817:1998–2004. doi: 10.1016/j.bbabio.2012.06.006
Kawakami K, Umena Y, Iwai M, et al. (2011) Roles of PsbI and PsbM in photosystem II dimer formation and stability studied by deletion mutagenesis and X-ray crystallography. Biochim Biophys Acta 1807:319–325. doi: 10.1016/j.bbabio.2010.12.013
Kern J, LOLL B, LĂ¼neberg C, et al. (2005) Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim Biophys Acta 1706:147–157. doi: 10.1016/j.bbabio.2004.10.007
Khan S, Sun JS, Brudvig GW (2015) Cation effects on the electron-acceptor side of Photosystem II. J Phys Chem B 119:7722–7728. doi: 10.1021/jp513035u
Kirilovsky D, Rutherford AW, Etienne AL (1994) Influence of DCMU and ferricyanide on photodamage in photosystem II. Biochemistry 33:3087–3095. doi: 10.1021/bi00176a043
Kiseleva LL, HorvĂƒth I, Vigh LS, Los DA (1999) Temperature-induced specific lipid desaturation in the thermophilic cyanobacterium Synechococcus vulcanus. FEMS Microbiology Letters 175:179–183. doi: 10.1111/j.1574-6968.1999.tb13617.x
Koike H, Yoneyama K, Kashino Y, Satoh K (1996) Mechanism of Electron Flow through the QB Site in Photosystem II. 4. Reaction Mechanism of Plastoquinone Derivatives at the QB Site in Spinach Photosystem II Membrane Fragments. Plant Cell Physiol 37:983–988. doi: 10.1093/oxfordjournals.pcp.a029048
KĂ³s PB, DeĂ¡k Z, Cheregi O, Vass I (2008) Differential regulation of psbA and psbD gene expression, and the role of the different D1 protein copies in the cyanobacterium Thermosynechococcus elongatus BP-1. Biochim Biophys Acta 1777:74–83. doi:10.1016/j.bbabio.2007.10.015
Koua FHM, Umena Y, Kawakami K, Shen J-R (2013) Structure of Sr-substituted photosystem II at 2.1 Å resolution and its implications in the mechanism of water oxidation. P Natl Acad Sci USA 110:3889–3894. doi: 10.1073/pnas.1219922110
Krieger A, Rutherford AW, Johnson GN (1995) On the determination of redox midpoint potential of the primary quinone electron acceptor, QA, in Photosystem II. BBA – Bioenergetics 1229:193–201. doi: 10.1016/0005-2728(95)00002-Z
Krieger-Liszkay A, Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 37:17339–17344. doi: 10.1021/bi9822628
Lambreva MD, Russo D, Polticelli F, et al. (2014) Structure/Function/Dynamics of Photosystem II Plastoquinone Binding Sites. Curr Protein Pept Sci 15:285–295.
Larom S, Salama F, Schuster G, Adir N (2010) Engineering of an alternative electron transfer path in photosystem II. P Natl Acad Sci USA 107:9650–9655. doi: 10.1073/pnas.1000187107
Larom S, Kallmann D, Saper G, et al. (2015) The Photosystem II D1-K238E mutation enhances electrical current production using cyanobacterial thylakoid membranes in a bio-photoelectrochemical cell. Photosynth Res 126:161–169. doi: 10.1007/s11120-015-0075-3
Lavergne J (1982) Mode of action of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. Evidence that the inhibitor competes with plastoquinone for binding to a common site on the acceptor side of Photosystem II. BBA – Bioenergetics 682:345–353. doi:10.1016/0005-2728(82)90048-2
Leng J, Sakurai I, Wada H, Shen J-R (2008) Effects of phospholipase and lipase treatments on photosystem II core dimer from a thermophilic cyanobacterium. Photosynth Res 98:469–478. doi: 10.1007/s11120-008-9335-9
Maly J, MasojĂdek J, Masci A, et al. (2005) Direct mediatorless electron transport between the monolayer of photosystem II and poly(mercapto-p-benzoquinone) modified gold electrode—new design of biosensor for herbicide detection. Biosens Bioelectron 21:923–932. doi: 10.1016/j.bios.2005.02.013
McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483. doi: 10.1021/cr0204294
Miles D, Bolen P, Farag S, et al. (1973) Hg++ − A DCMU independent electron acceptor of Photosystem II. Biochem Biophys Res Co 50:1113–1119.
Miller AF, Brudvig GW (1991) A guide to electron paramagnetic resonance spectroscopy of Photosystem II membranes. BBA – Bioenergetics 1056:1–18. doi:10.1016/S0005-2728(05)80067-2
Mizusawa N, Wada H (2012) The role of lipids in photosystem II. BBA – Bioenergetics 1817:194–208. doi: 10.1016/j.bbabio.2011.04.008
Mohanty N, Vass I, Demeter S (1989) Impairment of photosystem 2 activity at the level of secondary quinone electron acceptor in chloroplasts treated with cobalt, nickel and zinc ions. Physiol Plant 76:386–390. doi: 10.1111/j.1399-3054.1989.tb06208.x
MĂ¼h F, Zouni A (2013) The nonheme iron in photosystem II. Photosynth Res 116:295–314. doi: 10.1007/s11120-013-9926-y
Mulo P, Sakurai I, Aro E-M (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: From transcription to PSII repair. BBA – Bioenergetics 1817:247–257. doi: 10.1016/j.bbabio.2011.04.011
Oettmeier W (1999) Herbicide resistance and supersensitivity in photosystem II. Cell Mol Life Sci 55:1255–1277. doi: 10.1007/s000180050370
Ohad I, Dal Bosco C, Herrmann RG, Meurer J (2004) Photosystem II proteins PsbL and PsbJ regulate electron flow to the plastoquinone pool. Biochemistry-US 43:2297–2308. doi: 10.1021/bi0348260
Ohnishi N, Kashino Y, Satoh K, et al. (2006) Chloroplast-encoded polypeptide PsbT Is Involved in the repair of primary electron acceptor QA of Photosystem II during photoinhibition in Chlamydomonas reinhardtii. J Biol Chem 282:7107–7115. doi: 10.1074/jbc.M606763200
Pagliano C, Saracco G, Barber J (2013) Structural, functional and auxiliary proteins of photosystem II. Photosynth Res 116:167–188. doi: 10.1007/s11120-013-9803-8
Petrouleas V, Diner BA (1987) Light-induced oxidation of the acceptor-side Fe(II) of Photosystem II by exogenous quinones acting through the QB binding site. I. Quinones, kinetics and pH-dependence. BBA – Bioenergetics 893:126–137. doi: 10.1016/0005-2728(87)90032-6
Rao KK, Hall DO, Vlachopoulos N, et al. (1990) Photoelectrochemical responses of photosystem II particles immobilized on dye-derivatized TiO2 films. J Photoch Photobio B 5:379–389. doi: 10.1016/1011-1344(90)85052-X
Regel RE, Ivleva NB, Zer H, et al. (2001) Deregulation of electron flow within photosystem II in the absence of the PsbJ protein. J Biol Chem 276:41473–41478. doi: 10.1074/jbc.M102007200
Shevela D, Messinger J (2012) Probing the turnover efficiency of photosystem II membrane fragments with different electron acceptors. Biochim Biophys Acta 1817:1208–1212. doi: 10.1016/j.bbabio.2012.03.038
Shibamoto T, Kato Y, Sugiura M, Watanabe T (2009) Redox Potential of the Primary Plastoquinone Electron Acceptor QA in Photosystem II from Thermosynechococcus elongatus Determined by Spectroelectrochemistry. Biochemistry-US 48:10682–10684. doi: 10.1021/bi901691j
Shinopoulos KE, Brudvig GW (2012) Cytochrome b559 and cyclic electron transfer within Photosystem II. BBA – Bioenergetics 1817:66–75. doi:10.1016/j.bbabio.2011.08.002
Sigfridsson KGV, Bernat G, Mamedov F, Styring S (2004) Molecular interference of Cd2+ with Photosystem II. BBA – Bioenergetics 1659:19–31. doi: 10.1016/j.bbabio.2004.07.003
Suga M, Akita F, Hirata K, et al. (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517:99–103. doi: 10.1038/nature13991
Sugiura M, Inoue Y (1999) Highly purified thermo-stable oxygen-evolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol 40:1219–1231.
Takahashi R, Hasegawa K, Takano A, Noguchi T (2010) Structures and binding sites of phenolic herbicides in the QB pocket of photosystem II. Biochemistry-US 49:5445–5454. doi: 10.1021/bi100639q
Takasaka K, Iwai M, Umena Y, et al. (2010) Structural and functional studies on Ycf12 (Psb30) and PsbZ-deletion mutants from a thermophilic cyanobacterium. BBA – Bioenergetics 1797:278–284. doi: 10.1016/j.bbabio.2009.11.001
Tanaka A, Fukushima Y, Kamiya N (2017) Two different structures of the oxygen-evolving complex in the same polypeptide frameworks of photosystem II. J Am Chem Soc 139:1718–1721. doi: 10.1021/jacs.6b09666
Trebst A (2007) Inhibitors in the functional dissection of the photosynthetic electron transport system. Photosynth Res 92:217–224. doi: 10.1007/s11120-007-9213-x
Ulas G, Brudvig GW (2011) Redirecting Electron Transfer in Photosystem II from Water to Redox-Active Metal Complexes. J Am Chem Soc 133:13260–13263. doi: 10.1021/ja2049226
Umena Y, Kawakami K, Shen J-R, Kamiya N (2012) Crystal structure of oxygen-evolving Photosystem II at a resolution of 1.9 Å. Nature 473:55–60. doi: 10.1038/nature09913
Van Rensen J, van der Vet W, van Vliet W (1977) Inhibition and uncoupling of electron transport in isolated chloroplasts by the herbicide 4,6-dinitro-o-cresol. Photochem Photobiol 25:579–583.
Vinyard DJ, Ananyev GM, Dismukes GC (2013a) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 82:577–606. doi: 10.1146/annurev-biochem-070511-100425
Vinyard DJ, Gimpel J, Ananyev GM, et al. (2013b) Natural Variants of Photosystem II Subunit D1 Tune Photochemical Fitness to Solar Intensity. J Biol Chem 288:5451–5462. doi: 10.1074/jbc.M112.394668
Vogt L, Vinyard DJ, Khan S, Brudvig GW (2015) Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks. Curr Opin Chem Bio 25:152–158. doi: 10.1016/j.cbpa.2014.12.040
Wada H, Murata N (2010) Lipids in thylakoid Membranes and Photosynthetic Cells. In: Lipids in Photosynthesis. Springer Netherlands, Dordrecht, pp 1–9
Yehezkeli O, Tel-Vered R, Michaeli D, et al. (2013) Photosynthetic reaction center-functionalized electrodes for photo-bioelectrochemical cells. Photosynth Res 120:71–85. doi: 10.1007/s11120-013-9796-3
Yruela I, Montoya G, Alonso PJ, Picorel R (1991) Identification of the pheophytin-QA-Fe domain of the reducing side of the photosystem II as the Cu(II)-inhibitory binding site. J Biol Chem 266:22847–22850.
Zhang Y, Magdaong N, Frank HA, Rusling JF (2013) Protein film voltammetry and co-factor electron transfer dynamics in spinach photosystem II core complex. Photosynth Res 120:153–167. doi: 10.1007/s11120-013-9831-4
Zhu Z, Su Y, Li J, et al. (2009) Highly sensitive electrochemical sensor for mercury(II) ions by using a mercury-specific oligonucleotide probe and gold nanoparticle-based amplification. Anal Chem 81:7660–7666. doi: 10.1021/ac9010809
Zouni A, Witt HT, Kern J, et al. (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743. doi: 10.1038/35055589
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Wiwczar, J., Brudvig, G.W. (2017). Alternative Electron Acceptors for Photosystem II. In: Hou, H., Najafpour, M., Moore, G., Allakhverdiev, S. (eds) Photosynthesis: Structures, Mechanisms, and Applications. Springer, Cham. https://doi.org/10.1007/978-3-319-48873-8_4
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