Abstract
This review presents a broad overview of the research that enabled the structure determination of the bacterial reaction centers from Blastochloris viridis and Rhodobacter sphaeroides, with a focus on the contributions from Duysens, Clayton, and Feher. Early experiments performed in the laboratory of Duysens and others demonstrated the utility of spectroscopic techniques and the presence of photosynthetic complexes in both oxygenic and anoxygenic photosynthesis. The laboratories of Clayton and Feher led efforts to isolate and characterize the bacterial reaction centers. The availability of well-characterized preparations of pure and stable reaction centers allowed the crystallization and subsequent determination of the structures using X-ray diffraction. The three-dimensional structures of reaction centers revealed an overall arrangement of two symmetrical branches of cofactors surrounded by transmembrane helices from the L and M subunits, which also are related by the same twofold symmetry axis. The structure has served as a framework to address several issues concerning bacterial photosynthesis, including the directionality of electron transfer, the properties of the reaction center-cytochrome c 2 complex, and the coupling of proton and electron transfer. Together, these research efforts laid the foundation for ongoing efforts to address an outstanding question in oxygenic photosynthesis, namely the molecular mechanism of water oxidation.
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Abbreviations
- P865:
-
Bacteriochlorophyll dimer in reaction centers from R. sphaeroides
- BChl:
-
Bacteriochlorophyll
- BPhe:
-
Bacteriopheophytin
- P680:
-
Primary electron donor in photosystem II
- QB :
-
Secondary quinone
- EPR:
-
Electron paramagnetic resonance
- ENDOR:
-
Electron nuclear double resonance
References
Adir N, Axelrod HL, Beroza P, Isaacson RA, Rongey SH, Okamura MY, Feher G (1996) Co-crystallization and characterization of the photosynthetic reaction center–cytochrome c 2 complex from Rhodobacter sphaeroides. Biochemistry 35:2535–2547
Allen JP, Feher G (1984) Crystallization of reaction center from Rhodopseudomonas sphaeroides: preliminary characterization. Proc Nat Acad Sci USA 81:4795–4799
Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987a) Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proc Natl Acad Sci USA 84:5730–5734
Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987b) Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci USA 84:6162–6166
Allen JP, Artz K, Lin X, Williams JC, Ivancich A, Albouy D, Mattioli TA, Fetsch A, Kuhn M, Lubitz W (1996) Effects of hydrogen bonding to a bacteriochlorophyll-bacteriopheophytin dimer in reaction centers from Rhodobacter sphaeroides. Biochemistry 35:6612–6619
Allen JP, Olson TL, Oyala P, Lee WJ, Tufts AA, Williams JC (2012) Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers. Proc Natl Acad Sci USA 109:2314–2318
Arnold W, Clayton RK (1960) The first step in photosynthesis: evidence for its electronic nature. Proc Natl Acad Sci USA 46:769–776
Autenrieth F, Tajkhorshid E, Schulten K, Luthey-Schulten Z (2004) Role of water in transient cytochrome c 2 docking. J Phys Chem B 108:20376–20387
Axelrod HL, Okamura MY (2005) The structure and function of the cytochrome c 2: reaction center electron transfer complex from Rhodobacter sphaeroides. Photosyn Res 85:101–114
Axelrod HL, Feher G, Allen JP, Chirino AC, Day MW, Hsu BT, Rees DC (1994) Crystallization and X-ray structure determination of cytochrome c 2 from Rhodobacter sphaeroides in three crystal forms. Acta Cryst D 50:596–602
Axelrod HL, Abresch EC, Paddock ML, Okamura MY, Feher G (2000) Determination of the binding sites of the proton transfer inhibitors Cd2+ and Zn2+ in bacterial reaction centers. Proc Natl Acad Sci USA 97:1542–1547
Axelrod HL, Abresch EC, Okamura MY, Yeh AP, Rees DC, Feher G (2002) X-ray structure determination of the cytochrome c 2: reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol 319:501–515
Barnes CR (1893) On the food of green plants. Bot Gar 18:403–411
Blankenship RE (2002) Molecular mechanisms of photosynthesis. Kluwer Academic, Dordrecht
Blankenship R, Madigan MT, Bauer CE (eds) (1995) Anoxygenic photosynthetic bacteria. Kluwer Academic, Dordrecht
Bolton JR, Clayton RK, Reed DW (1969) An identification of the radical giving rise to the light-induced electron spin resonance signal in photosynthetic bacteria. Photochem Photobiol 9:209–218
Breton J, Martin JL, Migus A, Antonetti A, Orszag A (1986) Femtosecond spectroscopy of excitation energy transfer and initial charge separation in the reaction center of the photosynthetic bacterium Rhodopseudomonas viridis. Proc Natl Acad Sci USA 83:5121–5125
Bylina EJ, Youvan DC (1988) Directed mutations affecting spectroscopic and electron transfer properties of the primary donor in the photosynthetic reaction center. Proc Natl Acad Sci USA 85:7226–7230
Carter B, Boxer SG, Holten D, Kirmaier C (2012) Photochemistry of a bacterial photosynthetic reaction center missing the initial bacteriochlorophyll electron acceptor. J Phys Chem B 116:9971–9982
Chance B, Nishimura M (1960) On the mechanism of chlorophyll-cytochrome interaction: the temperature insensitivity of light-induced cytochrome oxidation in Chromatium. Proc Natl Acad Sci USA 46:19–24
Chance B, Smith L (1955) Respiratory pigments of Rhodospirillum rubrum. Nature 175:803–806
Chang CH, El-Kabbani O, Tiede D, Norris JR, Schiffer M (1991) Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 30:5352–5360
Clayton RK (1963) Toward the isolation of a photochemical reaction center in Rhodopseudomonas spheroides. Biochim Biophys Acta 75:312–323
Clayton RK (1988) Memories of many lives. Photosynth Res 19:207–224
Clayton RK (2002) Research on photosynthetic reaction centers from 1932 to 1987. Photosynth Res 73:63–71
Clayton RK, Smith C (1960) Rhodopseudomonas spheroides: high catalase and blue-green double mutants. Biochem Biophys Res Commun 3:143–145
Clayton RK, Wang RT (1971) Photochemical reaction centers from Rhodopseudomonas spheroides. Methods Enzymol 23:696–704
Cogdell RJ, Isaacs NW, Howard TD, McLuskey K, Fraser NJ, Prince SM (1999) How photosynthetic bacteria harvest solar energy. J Bacteriol 181:3869–3879
Crofts AR, Wraight CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726:149–185
Debus RJ (2001) Amino acid residues that modulate the properties of tyrosine YZ and the manganese cluster in the water oxidizing complex of photosystem II. Biochim Biophys Acta 1503:164–186
Debus RJ, Feher G, Okamura MY (1985) LM complex of reaction centers from Rhodopseudomonas sphaeroides R-26: characterization and reconstitution with the H subunit. Biochemistry 24:2488–2500
Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318:618–624
Deisenhofer J, Epp O, Sinning I, Michel H (1995) Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 246:429–457
Duysens LNM (1951) Transfer of light energy within the pigment systems present in photosynthesizing cells. Nature 168:548–550
Duysens LNM (1952) Transfer of excitation energy in photosynthesis. The University of Utrecht, Utrecht
Duysens LNM (1954) Reversible changes in the absorption spectrum of Chlorella upon irradiation. Science 120:353–354
Duysens LNM (1989) The study of reaction centers and of the primary and associated reactions of photosynthesis by means of absorption difference spectrophotometry: a commentary. Biochim Biophys Acta 1000:395–400
Duysens LNM, Amesz J, Kamp BM (1961) Two photochemical systems in photosynthesis. Nature 190:510–511
Emerson R, Arnold W (1932) The photochemical reaction in photosynthesis. J Gen Physiol 16:191–205
Emerson R, Chalmers R, Cederstrand C (1957) Some factors influencing the long-wave limit of photosynthesis. Proc Natl Acad Sci USA 43:133–143
Feher G (1971) Some chemical and physical properties of a bacterial reaction center particle and its primary photochemical reactants. Photochem Photobiol 14:373–387
Feher G (1998) Three decades of research in bacterial photosynthesis and the road leading to it: a personal account. Photosynth Res 55:1–40
Feher G, Okamura MY (1978) Chemical composition and properties of reaction centers. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum, New York/London, pp 349–386
Feher G, Hoff AJ, Isaacson RA, Ackerson LC (1975) ENDOR experiments on chlorophyll and bacteriochlorophyll in vitro and in the photosynthetic unit. Ann NY Acad Sci USA 244:239–259
Feher G, Allen JP, Okamura MY, Rees DC (1989) Structure and function of bacterial photosynthetic reaction centres. Nature 339:111–116
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838
Gest H (2006) History of the word photosynthesis and evolution of its definition. In: Beatty T, Gest H, Allen JF, Govindjee (eds) Discoveries in photosynthesis. Springer, Dordecht, pp 39–42
Govindjee, Beatty T, Gest H, Allen JF (eds) (2006) Discoveries in photosynthesis. Springer, Dordecht
Heller BA, Holten D, Kirmaier C (1995) Control of electron transfer between the L- and M-sides of photosynthetic reaction centers. Science 269:940–945
Hill R, Bendall F (1960) Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature 186:136–137
Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) (2009) The purple phototrophic bacteria. Springer, Dordrecht, Heidelberg
Joliot P, Barbieri G, Chabaud R (1969) Un nouveaux modele des centres photochimiques du système II. Photochem Photobiol 10:309–329
Kellogg EC, Kolaczkowski S, Wasielewski MR, Tiede DM (1984) Measurement of the extent of electron transfer to the bacteriopheophytin in the M-subunit in reaction centers of Rhodopseudomonas viridis. Photosynth Res 22:47–59
Kirmaier C, Holten D (1987) Primary photochemistry of reaction centers from the photosynthetic purple bacteria. Photosynth Res 13:225–260
Kirmaier C, Holten D, Bylina EJ, Youvan DC (1988) Electron transfer in a genetically modified bacterial reaction center containing a heterodimer. Proc Natl Acad Sci USA 85:7562–7566
Kirmaier C, Gaul D, DeBey R, Holten D, Schenck CC (1991) Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin. Science 251:922–927
Kok B, Forbuch B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution: a linear four step mechanism. Photochem Photobiol 11:457–475
Loach PA, Sekura DL (1967) A comparison of decay kinetics of photo-produced absorbance, EPR, and luminescence changes in chromatophores of Rhodospirillum rubrum. Photochem Photobiol 6:381–393
Lockhart DJ, Kirmaier C, Holten D, Boxer SG (1990) Electric field effects on the initial electron-transfer kinetics in bacterial photosynthetic reaction centers. J Phys Chem 94:6987–6995
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044
McDowell LM, Gaul D, Kirmaier C, Holten D, Schenck CC (1991) Investigation into the source of electron transfer asymmetry in bacterial reaction centers. Biochemistry 30:8315–8322
McElroy D, Feher G, Mauzerall DC (1969) On the nature of the free radical formed during the primary process of bacterial photosynthesis. Biochim Biophys Acta 172:180–183
McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483
Michel H (1982) Three-dimensional crystals of a membrane protein complex: the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 158:567–572
Michel H (1983) Crystallization of membrane proteins. Trends Biol Sci 8:56–59
Michel H, Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of Photosystem II. Biochemistry 27:1–7
Miyashita O, Onuchic JN, Okamura MY (2004) Transition state and encounter complex for fast association of cytochrome c 2 with bacterial reaction center. Proc Natl Acad Sci USA 101:16174–16179
Miyashita O, Okamura MY, Onuchic JN (2005) Interprotein electron transfer from cytochrome c 2 to photosynthetic reaction center: tunneling across an aqueous interface. Proc Natl Acad Sci USA 102:3558–3563
Nanba O, Satoh K (1987) Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559. Proc Natl Acad Sci USA 84:109–112
Norris JR, Uphaus RA, Crespi HL, Katz JJ (1971) Electron spin resonance of chlorophyll and the origin of signal I in photosynthesis. Proc Natl Acad Sci USA 68:625–628
Norris JR, Scheer H, Katz JJ (1975) Models for antenna and reaction center chlorophylls. Ann NY Acad Sci USA 244:260–280
Okamura MY, Feher G (1995) Proton-coupled electron transfer reactions of QB in reaction centers from photosynthetic bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 577–594
Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458:148–163
Paddock ML, Rongey SH, Feher G, Okamura MY (1989) Pathway of proton transfer in bacterial reaction centers: replacement of glutamic acid 212 in the L subunit by glutamine inhibits quinone (secondary acceptor) turnover. Proc Natl Acad Sci USA 86:6602–6606
Paddock ML, Rongey SH, McPherson PH, Juth A, Feher G, Okamura MY (1994) Pathway of proton transfer in bacterial reaction centers: role of aspartate L213 in proton transfers associated with reduction of quinone to dihydroquinone. Biochemistry 33:734–745
Parson WW (1968) The role of P870 in bacterial photosynthesis. Biochim Biophys Acta 153:248–259
Rappaport F, Diner BA (2008) Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coord Chem Rev 252:259–272
Reed DW, Clayton RK (1968) Isolation of a reaction center fraction from Rhodopseudomonas spheroides. Biochem Biophys Res Commun 30:471–475
Rivalta I, Brudvig GW, Batista VS (2012) Oxomanganese complexes for natural and artificial photosynthesis. Curr Opin Chem Biol 16:11–18
Salemme FR, Freer ST, Xuong NH, Alden RA, Kraut J (1973) The structure of oxidized cytochrome c 2 of Rhodospirillum rubrum. J Biol Chem 248:3910–3921
Stowell MHB, McPhillips TM, Rees DC, Soltis SM, Abresch E, Feher G (1997) Light-induced structural changes in photosynthetic reaction center: implication for mechanism of electron-proton transfer. Science 276:812–816
Sutton MR, Rosen D, Feher G, Steiner LA (1982) Amino-terminal sequences of the L, M and H subunits of reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides R-26. Biochemistry 21:3842–3849
Takahashi E, Wraight CA (1990) A crucial role for Asp L213 in the proton transfer pathway to the secondary quinone of reaction centers from Rhodobacter sphaeroides. Biochim Biophys Acta 1020:107–111
Takahashi E, Wraight CA (1991) Small weak acids stimulate proton transfer events in site-directed mutants of the two ionizable residues, Glu L212 and Asp L213, in the QB-binding site of Rhodobacter sphaeroides reaction center. FEBS Lett 283:140–144
Thielges M, Uyeda G, Camara-Artigas A, Kálmán L, Williams JC, Allen JP (2005) Design of a redox-linked active metal site: manganese bound to bacterial reaction centers at a site resembling that of photosystem II. Biochemistry 44:7389–7394
Tiede DM (1987) Cytochrome c orientation in electron-transfer complexes with photosynthetic reaction centers of Rhodobacter sphaeroides and when bound to the surface of negatively charged membranes: characterization by optical linear dichroism. Biochemistry 26:397–410
Tommos C, Babcock GT (2000) Proton and hydrogen currents in photosynthetic water oxidation. Biochim Biophys Acta 1458:199–219
Trebst A (1987) The three-dimensional structure of the herbicide binding niche on the reaction center polypeptides of Photosystem II. Z Naturforsch C 42:742–750
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–61
Utschig LM, Ohigashi Y, Thurnauer MC, Tiede DM (1998) A new metal-binding site in photosynthetic bacterial reaction centers that modulates QA to QB electron transfer. Biochemistry 37:8278–8281
van Grondelle R, Holmes NG, Rademaker H, Duysens LNM (1978) Bacteriochlorophyll fluorescence of purple bacteria at low redox potentials: the relationship between reaction center triplet yield and the emission yield. Biochim Biophys Acta 503:10–25
Vernon LP, Kamen MD (1953) Studies on the metabolism of photosynthetic bacteria. XV. Photoautooxidation of ferrocytochrome c in extracts of Rhodospirillum rubrum. Arch Biochem Biophys 44:298–311
Wang H, Lin S, Allen JP, Williams JC, Blankert S, Laser C, Woodbury NW (2007) Protein dynamics control the kinetics of initial electron transfer in photosynthesis. Science 316:747–750
Williams JC, Taguchi AKW (1995) Genetic manipulation of purple photosynthetic bacteria. In: Blankenship RE, Madigan MT, Bauer C (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic, Dordrecht, pp 1029–1065
Williams JC, Steiner LA, Ogden RC, Simon MI, Feher G (1983) Primary structure of the M subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 80:6505–6509
Williams JC, Steiner LA, Feher G, Simon MI (1984) Primary structure of the L subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 81:7303–7307
Williams JC, Steiner LA, Feher G (1986) Primary structure of the reaction center from Rhodopseudomonas sphaeroides. Proteins 1:312–325
Woodbury NW, Allen J (1995) The pathway and thermodynamics of electron transfer in wild type and mutant reaction centers of purple non sulfur bacteria. In: Blankenship RE, Madigan MT, Bauer C (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic, Dordrecht, pp 527–557
Wraight CA, Gunner MR (2009) The acceptor quinones of purple photosynthetic bacteria- structure and spectroscopy. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The purple phototrophic bacteria. Plenum, New York, pp 379–405
Wydrzynski TJ, Satoh K (eds) (2005) Photosystem II: The light-induced water: plastoquinone oxidoreductase. Springer, Dordrecht
Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y, Biesiadka J, Loll B, Saenger W, Messinger J, Zouni A, Yachandra VK (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314:821–825
Yeates TO, Komiya H, Rees DC, Allen JP, Feher G (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: membrane-protein interactions. Proc Natl Acad Sci USA 84:6438–6442
Youvan DC, Bylina EJ, Alberti M, Begusch H, Hearst JE (1984) Nucleotide and deduced polypeptide sequences of the photosynthetic reaction center, B870 antenna, and flanking polypeptides from R. capsulata. Cell 37:949–957
Zinth W, Wachtveitl J (2005) The first picoseconds in bacterial photosynthesis- ultrafast electron transfer for the efficient conversion of light energy. ChemPhysChem 6:871–880
Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743
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This work was supported by the Grant CHE 1158552 from the National Science Foundation.
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Olson, T.L., Williams, J.C. & Allen, J.P. The three-dimensional structures of bacterial reaction centers. Photosynth Res 120, 87–98 (2014). https://doi.org/10.1007/s11120-013-9821-6
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DOI: https://doi.org/10.1007/s11120-013-9821-6