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Consequences of saturation mutagenesis of the protein ligand to the B-side monomeric bacteriochlorophyll in reaction centers from Rhodobacter capsulatus

  • Kaitlyn M. Faries
  • Claire E. Kohout
  • Grace Xiyu Wang
  • Deborah K. Hanson
  • Dewey Holten
  • Philip D. Laible
  • Christine KirmaierEmail author
Original Article
  • 38 Downloads

Abstract

In bacterial reaction centers (RCs), photon-induced initial charge separation uses an A-side bacteriochlorophyll (BChl, BA) and bacteriopheophytin (BPh, HA), while the near-mirror image B-side BB and HB cofactors are inactive. Two new sets of Rhodobacter capsulatus RC mutants were designed, both bearing substitution of all amino acids for the native histidine M180 (M-polypeptide residue 180) ligand to the core Mg ion of BB. Residues are identified that largely result in retention of a BChl in the BB site (Asp, Ser, Pro, Gln, Asn, Gly, Cys, Lys, and Thr), ones that largely harbor the Mg-free BPh in the BB site (Leu and Ile), and ones for which isolated RCs are comprised of a substantial mixture of these two RC types (Ala, Glu, Val, Met and, in one set, Arg). No protein was isolated when M180 is Trp, Tyr, Phe, or (in one set) Arg. These findings are corroborated by ground state spectra, pigment extractions, ultrafast transient absorption studies, and the yields of B-side transmembrane charge separation. The changes in coordination chemistries did not reveal an RC with sufficiently precise poising of the redox properties of the BB-site cofactor to result in a high yield of B-side electron transfer to HB. Insights are gleaned into the amino acid properties that support BChl in the BB site and into the widely observed multi-exponential decay of the excited state of the primary electron donor. The results also have direct implications for tuning free energies of the charge-separated intermediates in RCs and mimetic systems.

Keywords

Electron transfer Pigment content Bacteriochlorophyll ligand M180 histidine Accessory bacteriochlorophyll B-side charge separation 

Abbreviations

RC

Reaction center

ET

Electron transfer

WT

Wild type

BChl

Bacteriochlorophyll

BPh

Bacteriopheophytin

P

Dimer of bacteriochlorophyll in the RC

P*

Lowest singlet excited state of P

BA

A-side monomeric bacteriochlorophyll

HA

A-side monomeric bacteriopheophytin

βA

A-side monomeric bacteriochlorophyll that replaces HA in RCs due to mutation of the native Leu residue at position 212 on the M polypeptide (LeuM212) to a His

QA

A-side ubiquinone

BB

B-side monomeric bacteriochlorophyll with native His ligand (HisM180)

ΦB

B-side monomeric bacteriopheophytin that replaces BB in some RCs depending on the amino acid substituted for native HisM180

HB

B-side monomeric bacteriopheophytin

QB

B-side ubiquinone

CarT

Carotenoid triplet excited state

PR

Triplet excited state of P

Notes

Acknowledgements

This work was supported by the U. S. Department of Energy, Office of Basic Energy Sciences under grant DE-CD0002036 (to CK and DH), and associated Field Work Proposal (to PDL). Argonne, a U. S. Department of Energy Office of Science laboratory is operated under Contract No. DE-AC02-06CH11357. KMF was supported in part by National Science Foundation Graduate Research Fellowship grant DGE-1143954.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (PDF 7702 KB)

References

  1. Alden RG, Parson WW, Chu ZT, Warshel A (1995) Calculations of electrostatic energies in photosynthetic reaction centers. J Am Chem Soc 117:12284–12298CrossRefGoogle Scholar
  2. Alden RG, Parson WW, Chu ZT, Warshel A (1996) Orientation of the OH dipole of tyrosine (M)210 and its effect on electrostatic energies in photosynthetic bacterial reaction centers. J Phys Chem 100:16761–16770CrossRefGoogle Scholar
  3. Allen JP, Feher G, Yeates TO, Komiya H, Rees DC (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Proc Natl Acad Sci USA 84:5730–5734CrossRefPubMedGoogle Scholar
  4. Arlt T, Dohse B, Schmidt S, Wachtveitl J, Laussermair E, Zinth W, Oesterhelt D (1996) Electron transfer dynamics of Rhodopseudomonas viridis reaction centers with a modified binding site for the accessory bacteriochlorophyll. Biochemistry 35:9235–9244CrossRefPubMedGoogle Scholar
  5. Beekman LMP et al (1995) Time-resolved and steady-state spectroscopic analysis of membrane-bound reaction centers from Rhodobacter sphaeroides: comparisons with detergent-solubilized complexes. Biochemistry 34:14712–14721CrossRefPubMedGoogle Scholar
  6. Beekman LMP et al (1996) Primary electron transfer in membrane-bound reaction centers with mutations at the M210 position. J Phys Chem 100:7256–7268 doi.  https://doi.org/10.1021/Jp953054h CrossRefGoogle Scholar
  7. Bixon M, Jortner J, Michel-Beyerle ME (1995) A kinetic analysis of the primary charge separation in bacterial photosynthesis. Energy gaps and static heterogeneity. Chem Phys 197:389–404CrossRefGoogle Scholar
  8. Breton J, Martin JL, Lambry JC, Robles SJ, Youvan DC (1990) Ground state and femtosecond transient absorption spectroscopy of a mutant of Rhodobacter capsulatus which lacks the initial electron acceptor bacteriopheophyrin. In: Michel-Beyerle ME (ed) Structure and function of bacterial photosynthetic reaction centers. Springer, New York, pp 293–302CrossRefGoogle Scholar
  9. Bylina EJ, Kirmaier C, McDowell LM, Holten D, Youvan DC (1988) Influence of an amino acid residue on the optical properties and electron transfer dynamics of a photosynthetic reaction center complex. Nature 336:182–184CrossRefGoogle Scholar
  10. Bylina EJ, Kolaczkowski SV, Norris JR, Youvan DC (1990) Epr characterization of genetically modified reaction centers of Rhodobacter-capsulatus. Biochemistry 29:6203–6210CrossRefPubMedGoogle Scholar
  11. 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.  https://doi.org/10.1021/Jp305276m CrossRefPubMedGoogle Scholar
  12. Chang C-H, El-Kabbani O, Tiede DM, Norris JR, Schiffer M (1991) The structure of the membrane-bound photosynthetic reaction center from Rhodobacter sphaeroides R-26. Proc Natl Acad Sci USA 30:5352–5360Google Scholar
  13. Chuang JI, Boxer SG, Holten D, Kirmaier C (2006) High yield of M-side electron transfer in mutants of Rhodobacter capsulatus reaction centers lacking the L-side bacteriopheophytin. Biochemistry 45:3845–3851CrossRefPubMedGoogle Scholar
  14. Chuang JI, Boxer SG, Holten D, Kirmaier C (2008) Temperature dependence of electron transfer to the M-side bacteriopheophytin in Rhodobacter capsulatus reaction centers. J Phys Chem B 112:5487–5499CrossRefPubMedGoogle Scholar
  15. Cotton TM, Van Duyne RP (1979) Electrochemical investigation of the redox properties of bacteriochlorophyll and bacteriopheophytin in aprotic-solvents. J Am Chem Soc 101:7605–7612.  https://doi.org/10.1021/Ja00519a023 CrossRefGoogle Scholar
  16. de Boer AL, Neerken S, de Wijn R, Permentier HP, Gast P, Vijgenboom E, Hoff AJ (2002a) B-branch electron transfer in reaction centers of Rhodobacter sphaeroides assessed with site-directed mutagenesis. Photosynth Res 71:221–239CrossRefPubMedGoogle Scholar
  17. de Boer AL, Neerken S, de Wijn R, Permentier HP, Gast P, Vijgenboom E, Hoff AJ (2002b) High yield of B-branch electron transfer in a quadruple reaction center mutant of the photosynthetic bacterium Rhodobacter sphaeroides. Biochemistry 41:3081–3088CrossRefPubMedGoogle Scholar
  18. Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center from Rhodopseudomonas viridis at 3 Å resolution. Nature 318:618–624CrossRefPubMedGoogle Scholar
  19. Du M et al (1992) Femtosecond spontaneous-emission studies of reaction centers from photosynthetic bacteria. Proc Natl Acad Sci USA 89:8517–8521CrossRefPubMedGoogle Scholar
  20. Dylla NP et al (2016) Species differences in unlocking B-side electron transfer in bacterial reaction centers. FEBS Lett 590:2515–2526.  https://doi.org/10.1002/1873-3468.12015 CrossRefPubMedGoogle Scholar
  21. Ermler U, Fritsch G, Buchanan SK, Michel H (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 A resolution: cofactors and protein-cofactor interactions. Structure 2:925–936CrossRefPubMedGoogle Scholar
  22. Fajer J, Borg DC, Forman A, Dolphin D, Felton RH (1973) Anion radical of bacteriochlorophyll. J Am Chem Soc 95:2739–2741.  https://doi.org/10.1021/Ja00789a085 CrossRefPubMedGoogle Scholar
  23. Fajer J, Brune DC, Davis MS, Forman A, Spaulding LD (1975) Primary charge separation in bacterial photosynthesis: oxidized chlorophylls and reduced pheophytin. Proc Natl Acad Sci USA 72:4956–4960CrossRefPubMedGoogle Scholar
  24. Faries KM et al (2016) Optimizing multi-step B-side charge separation in photosynthetic reaction centers from Rhodobacter capsulatus. Biochim Biophys Acta 1857:150–159.  https://doi.org/10.1016/j.bbabio.2015.11.013 CrossRefPubMedGoogle Scholar
  25. Faries KM, Kressel LL, Wander MJ, Holten D, Laible PD, Kirmaier C, Hanson DK (2012) High-throughput engineering to revitalize a vestigial electron transfer pathway in bacterial photosynthetic reaction centers. J Biol Chem 387:8507–8514 CrossRefGoogle Scholar
  26. Faries KM, Dylla NP, Hanson DK, Holten D, Laible PD, Kirmaier C (2017) Manipulating the energetics and rates of electron transfer in Rhodobacter capsulatus reaction centers with asymmetric pigment content. J Phys Chem B 121:6989–7004.  https://doi.org/10.1021/acs.jpcb.7b01389 CrossRefPubMedGoogle Scholar
  27. Felton RH (1978) Primary redox reactions of metalloporphyrins. In: Dolphin D (ed) The porphyrins, vol 5. Academic Press, New York, pp 53–125CrossRefGoogle Scholar
  28. Frolov D et al (2010) Structural and spectroscopic consequences of hexacoordination of a bacteriochlorophyll cofactor in the Rhodobacter sphaeroides reaction center. Biochemistry 49:1882–1892.  https://doi.org/10.1021/Bi901922t CrossRefPubMedGoogle Scholar
  29. Gehlen JN, Marchi M, Chandler D (1994) Dynamics affecting the primary charge transfer in photosynthesis. Science 263:499–502CrossRefPubMedGoogle Scholar
  30. Goldsmith JO, King B, Boxer SG (1996) Mg coordination by amino acid side chains is not required for assembly and function of the special pair in bacterial photosynthetic reaction centers. Biochemistry 35:2421–2428.  https://doi.org/10.1021/Bi9523365 CrossRefPubMedGoogle Scholar
  31. Gunner MR, Nicholls A, Honig B (1996) Electrostatic potentials in Rhodopseudomonas viridis reaction centers: implications for the driving force and directionality of electron transfer. J Phys Chem 100:4277–4291CrossRefGoogle Scholar
  32. Hamm P, Gray KA, Oesterhelt D, Feick R, Scheer H, Zinth W (1993) Subpicosecond emission studies of bacterial reaction centers. Biochim Biophys Acta 1142:99–105CrossRefGoogle Scholar
  33. Hartwich G, Lossau H, Michel-Beyerle ME, Ogrodnik A (1998) Nonexponential fluorescence decay in reaction centers of Rhodobacter sphaeroides reflecting dispersive charge separation up to 1 ns. J Phys Chem B 102:3815–3820CrossRefGoogle Scholar
  34. Heller BA, Holten D, Kirmaier C (1995) Control of electron transfer to the L-side versus the M-side of the photosynthetic reaction center. Science 269:940–945CrossRefPubMedGoogle Scholar
  35. Heller BA, Holten D, Kirmaier C (1996) Effects of Asp residues near the L-side pigments in bacterial reaction centers. Biochemistry 35:15418–15427CrossRefPubMedGoogle Scholar
  36. Holzwarth AR, Muller MG (1996) Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides. A femtosecond transient absorption study. Biochemistry 35:11802–11831CrossRefGoogle Scholar
  37. Huppman P et al (2002) Kinetics, energetics, and electronic coupling of the primary electron transfer reactions in mutated reaction centers of Blastochloris viridis. Biophys J 82:3186–3197CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kakitani Y, Hou A, Miyasako Y, Koyama Y, Nagae H (2010) Rates of the initial two steps of electron transfer in reaction centers from Rhodobacter sphaeroides as determined by singular-value decomposition followed by global fitting. Chem Phys Lett 492:142–149CrossRefGoogle Scholar
  39. Katilius E, Turanchik T, Lin S, Taguchi AKW, Woodbury NW (1999) B-side electron transfer in a Rhodobacter sphaeroides reaction center mutant in which the B-Side monomer bacteriochlorophyll is replaced with bacteriopheophytin. J Phys Chem B 103:7386–7389CrossRefGoogle Scholar
  40. Katilius E, Katiliene Z, Lin S, Taguchi AKW, Woodbury NW (2002a) B-side electron transfer in the HE(M182) reaction center mutant from Rhodobacter sphaeroides. J Phys Chem B 106:12344–12350.  https://doi.org/10.1021/jp026388x CrossRefGoogle Scholar
  41. Katilius E, Katiliene Z, Lin S, Taguchi AKW, Woodbury NW (2002b) B side electron transfer in a Rhodobacter sphaeroides reaction center mutant in which the B side monomer bacteriochlorophyll is replaced with bacteriopheophytin: low-temperature study and energetics of charge-separated states. J Phys Chem B 106:1471–1475.  https://doi.org/10.1021/jp013265o CrossRefGoogle Scholar
  42. Katilius E, Babendure JL, Katiliene Z, Lin S, Taguchi AKW, Woodbury NW (2003) Manipulations of the B-side charge-separated states’ energetics in the Rhodobacter sphaeroides reaction center. J Phys Chem B 107:12029–12034.  https://doi.org/10.1021/jp035013o CrossRefGoogle Scholar
  43. Katilius E, Babendure JL, Lin S, Woodbury NW (2004) Electron transfer dynamics in Rhodobacter sphaeroides reaction center mutants with a modified ligand for the monomer bacteriochlorophyll on the active side. Photosynth Res 81:165–180 doi.  https://doi.org/10.1023/B:Pres.0000035048.10358.90 CrossRefGoogle Scholar
  44. Kirmaier C, Holten D (1990) Evidence that a distribution of bacterial reaction centers underlies the temperature- and detection-wavelength-dependence of the rates of the primary electron transfer reactions. Proc Natl Acad Sci USA 97:3522–3556Google Scholar
  45. Kee HL, Laible PD, Bautista JA, Hanson DK, Holten D, Kirmaier C (2006) Determination of the rate and yield of B-side quinone reduction in Rhodobacter capsulatus RCs. Biochemistry 45:7314–7322CrossRefPubMedGoogle Scholar
  46. Kirmaier C, Gaul D, DeBey R, Holten D, Schenck CC (1991) Charge separation in a reaction center incorporating bacteriochlorophyll in place of photoactive bacteriopheophytin. Science 251:922–927CrossRefPubMedGoogle Scholar
  47. Kirmaier C, Laporte L, Schenck CC, Holten D (1995) The nature and dynamics of the charge-separated intermediate in reaction centers in which bacteriochlorophyll replaces the photoactive bacteriopheophytin. 2. The rates and yields of charge separation and recombination. J Phys Chem 99:8910–8917CrossRefGoogle Scholar
  48. Kirmaier C, Weems D, Holten D (1999) M-side electron transfer in reaction center mutants with a lysine near the nonphotoactive bacteriochlorophyll. Biochemistry 38:11516–11530CrossRefPubMedGoogle Scholar
  49. Kirmaier C, He C, Holten D (2001) Manipulating the direction of electron transfer in the bacterial reaction center by swapping Phe for Tyr Near BChlM (L181) and Tyr for Phe near BChlL (M208). Biochemistry 40:12132–12139CrossRefPubMedGoogle Scholar
  50. Kirmaier C, Cua A, He C, Holten D, Bocian DF (2002a) Probing M-branch electron transfer and cofactor environment in the bacterial photosynthetic reaction center by the addition of a hydrogen bond to the M-side bacteriopheophytin. J Phys Chem B 106:495–503CrossRefGoogle Scholar
  51. Kirmaier C, Laible PD, Czarnecki K, Hata AN, Hanson DK, Bocian DF, Holten D (2002b) Comparison of M-side electron transfer in Rb. sphaeroides and Rb. capsulatus reaction centers. J Phys Chem B 106:1799–1808CrossRefGoogle Scholar
  52. Kirmaier C, Laible PD, Hanson DK, Holten D (2003) B-side charge separation in bacterial photosynthetic reaction centers: nanosecond-timescale electron transfer from HB to QB. Biochemistry 42:2016–2024CrossRefPubMedGoogle Scholar
  53. Kirmaier C, Laible PD, Hanson DK, Holten D (2004) B-side electron transfer to form P+HB in reaction centers from the F(L181)Y/Y(M208)F mutant of Rhodobacter capsulatus. J Phys Chem B 108:11827–11832CrossRefGoogle Scholar
  54. Koepke J, Hu XC, Muenke C, Schulten K, Michel H (1996) The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4:581–597CrossRefPubMedGoogle Scholar
  55. Kressel L et al (2014) High yield of secondary B-side electron transfer in mutant Rhodobacter capsulatus reaction centers. Biochim Biophys Acta 1837:1892–1903CrossRefPubMedGoogle Scholar
  56. Laible PD, Greenfield SR, Wasielewski MR, Hanson DK, Pearlstein RM (1997) Antenna excited state decay kinetics establish primary electron transfer in reaction centers as heterogeneous. Biochemistry 36:8677–8685CrossRefPubMedGoogle Scholar
  57. Laible PD, Kirmaier C, Udawatte CSM, Hofman SJ, Holten D, Hanson DK (2003) Quinone reduction via secondary B-branch electron transfer in mutant bacterial reaction centers. Biochemistry 42:1718–1730CrossRefPubMedGoogle Scholar
  58. Laporte L, Kirmaier C, Schenck CC, Holten D (1995) Free-energy dependence of the rate of electron-transfer to the primary quinone in beta-type reaction centers. Chem Phys 197:225–237CrossRefGoogle Scholar
  59. Leonova MM, Vasilieva LG, Khatypov RA, Boichenko VA, Shuvalov VA (2009) Properties of mutant reaction centers of Rhodobacter sphaeroides with substitutions of histidine L153, the axial Mg(2+) ligand of bacteriochlorophyll B(A). Biochemistry 74:452–460.  https://doi.org/10.1134/S0006297909040142 PubMedGoogle Scholar
  60. Lin S, Taguchi AKW, Woodbury NW (1996) Excitation wavelength dependence of energy transfer and charge separation in reaction centers from Rhodobacter sphaeroides: evidence of adiabatic electron transfer. J Phys Chem 42:17067–17078CrossRefGoogle Scholar
  61. Lin S, Jackson J, Taguchi AKW, Woodbury NW (1998) Excitation wavelength dependent spectral evolution in Rhodobacter sphaeroides R-26 reaction centers at low temperatures: the Q Y transition region. J Phys Chem B 102:4016–4022CrossRefGoogle Scholar
  62. McLuskey K, Prince SM, Cogdell RJ, Isaacs NW (2001) The crystallographic structure of the B800–820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas acidophila strain 7050. Biochemistry 40:8783–8789CrossRefPubMedGoogle Scholar
  63. Michel-Beyerle ME (ed) (1996) The reaction center of photosynthetic bacteria. Springer, BerlinGoogle Scholar
  64. Morris ZS et al (2003) Lysine substitutions near photoactive cofactors in the bacterial photosynthetic reaction center have opposite effects on the rate of triplet energy transfer. Chem Phys 294:329–346CrossRefGoogle Scholar
  65. Muh F, Williams JC, Allen JP, Lubitz W (1998) A conformational change of the photoactive bacteriophyeophytin in reaction centers from Rhodobacter sphaeroides. Biochemistry 37:13066–13074CrossRefPubMedGoogle Scholar
  66. Muller MG, Griebenow K, Holzarth AR (1992) Primary processes in isolated bacterial reaction centers from Rhodobacter sphaeroides studied by picosecond fluorescence kinetics. Chem Phys Lett 199:465–469CrossRefGoogle Scholar
  67. Nabedryk E, Allen JP, Taguchi AKW, Williams JC, Woodbury NW, Breton J (1993) Fourier-transform infrared study of the primary electron-donor in chromatophores of Rhodobacter sphaeroides with reaction centers genetically-modified at residue-M160 and residue-L131. Biochemistry 32:13879–13885CrossRefPubMedGoogle Scholar
  68. Niwa S, Yu LJ, Takeda K, Hirano Y, Kawakami T, Wang-Otomo ZY, Miki K (2014) Structure of the LH1-RC complex from Thermochromatium tepidum at 3.0 angstrom. Nature 508:228–228+.  https://doi.org/10.1038/nature13197 CrossRefPubMedGoogle Scholar
  69. Oba T, Tamiaki H (2014) Asymmetry of chlorophylls in photosynthetic proteins: from the viewpoint of coordination chemistry. J Porphyrins Phthalocyanines 18:919–932.  https://doi.org/10.1142/S1088424614500710 CrossRefGoogle Scholar
  70. Ogrodnik A, Keupp W, Volk M, Aumeier G, Michel-Beyerle ME (1994) Inhomogeneity of radical pair energies in photosynthetic reaction centers revealed by differences in recombination dynamics of P+H when detected in delayed emission and in absorption. J Phys Chem 98:3432–3439CrossRefGoogle Scholar
  71. Paddock ML, Chang C, Xu Q, Abresch EC, Axelrod HL, Feher G, Okamura MY (2005) Quinone (QB) reduction by B-branch electron transfer in mutant bacterial reaction centers from Rhodobacter sphaeroides: quantum efficiency and X-ray structure. Biochemistry 44:6920–6928CrossRefPubMedGoogle Scholar
  72. Pan J, Saer RG, Lin S, Guo Z, Beatty JT, Woodbury NW (2013) The protein environment of the bacteriopheophytin anion modulates charge separation and charge recombination in bacterial reaction centers. J Phys Chem B 117:7179–7189CrossRefPubMedGoogle Scholar
  73. Pan J, Saer R, Lin S, Beatty JT, Woodbury NW (2016) Electron transfer in bacterial reaction centers with the photoactive bacteriopheophytin replaced by a bacteriochlorophyll through coordinating ligand substitution. Biochemistry 55:4909–4918.  https://doi.org/10.1021/acs.biochem.6b00317 CrossRefPubMedGoogle Scholar
  74. Parson WW, Chu ZT, Warshel A (1990) Electrostatic control of charge separation in bacterial photosynthesis. Biochim Biophys Acta 1017:251–272CrossRefPubMedGoogle Scholar
  75. Peloquin JM, Williams JC, Lin X, Alden RG, Taguchi AKW, Allen JP, Woodbury NW (1994) Time-dependent thermodynamics during early electron transfer in reaction centers from Rhodobacter sphaeroides. Biochemistry 33:8089–8100CrossRefPubMedGoogle Scholar
  76. Peloquin JM, Lin S, Taguchi AKW, Woodbury NW (1995) Excitation wavelength dependence of bacterial reaction-center photochemistry. 1. Ground-state and excited-state evolution. J Phys Chem 99:1349–1356CrossRefGoogle Scholar
  77. Peloquin JM, Lin S, Taguchi AKW, Woodbury NW (1996) Excitation wavelength dependence of bacterial reaction center photochemistry. 2. Low-temperature measurements and spectroscopy of charge separation. J Phys Chem 100:1428–14235CrossRefGoogle Scholar
  78. Prince SM, Papiz MZ, Freer AA, McDermott G, HawthornthwaiteLawless AM, Cogdell RJ, Isaacs NW (1997) Apoprotein structure in the LH2 complex from Rhodopseudomonas acidophila strain 10050: modular assembly and protein pigment interactions. J Mol Biol 268:412–423CrossRefPubMedGoogle Scholar
  79. Saer RG, Hardjasa A, Rosell FI, Mauk AG, Murphy MEP, Beatty JT (2013) Role of Rhodobacter sphaeroides photosynthetic reaction center residue M214 in the composition, absorbance properties, and conformations of H-A and B-A cofactors. Biochemistry 52:2206–2217CrossRefPubMedGoogle Scholar
  80. Saggu M et al (2014) Putative hydrogen bond to tyrosine M208 in photosynthetic reaction centers from Rhodobacter capsulatus significantly slows primary charge separation. J Phys Chem B 118:6721–6732CrossRefPubMedPubMedCentralGoogle Scholar
  81. Schmidt S et al (1994) Energetics of the primary electron transfer reaction revealed by ultrafast spectroscopy on modified bacterial reaction centers. Chem Phys Lett 223:116–120CrossRefGoogle Scholar
  82. Stanley RJ, Boxer SG (1995) Oscillations in the spontaneous fluorescence from photosynthetic reaction centers. J Phys Chem 99:859–863CrossRefGoogle Scholar
  83. Taguchi AK, Stocker JW, Alden RG, Causgrove TP, Peloquin JM, Boxer SG, Woodbury NW (1992) Biochemical characterization and electron-transfer reactions of sym1, a Rhodobacter capsulatus reaction center symmetry mutant which affects the initial electron donor. Biochemistry 31:10345–10355CrossRefPubMedGoogle Scholar
  84. van der Rest M, Gingras G (1974) Pigment complement of photosynthetic reaction center isolated from Rhodospirillum rubrum. J Biol Chem 249:6446–6453PubMedGoogle Scholar
  85. Volk M, Aumeier G, Langenbacher T, Feick R, Ogrodnik A, Michel-Beyerle ME (1998) Energetics and mechanism of primary charge separation in bacterial photosynthesis. A comparative study on reaction centers of Rhodobacter sphaeroides and Chloroflexus aurantiacus. J Phys Chem B 102:735–751CrossRefGoogle Scholar
  86. Vos MH, Lambry JC, Robles SJ, Youvan DC, Breton J, Martin JL (1991) Direct observation of vibrational coherence in bacterial reaction centers using femtosecond absorption spectroscopy. Proc Natl Acad Sci USA 88:8885–8889CrossRefPubMedGoogle Scholar
  87. Vos MH, Lambry JC, Robles SJ, Youvan DC, Breton J, Martin JL (1992) Femtosecond spectral evolution of the excited state of bacterial reaction centers at 10 K. Proc Natl Acad Sci USA 89:613–617CrossRefPubMedGoogle Scholar
  88. Wachtveitl J, Farchaus JW, Das R, Lutz M, Robert B, Mattioli TA (1993) Structure, spectroscopic, and redox properties of Rhodobacter sphaeroides reaction centers bearing point mutations near the primary electron donor. Biochemistry 32:12875–12886CrossRefPubMedGoogle Scholar
  89. Wang HY, 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 316:747–750CrossRefPubMedGoogle Scholar
  90. Warshel A, Chu ZT, Parson WW (1994) On the energetics of the primary electron-transfer process in bacterial reaction centers. J Photochem Photobiol A Chem 82:123–128CrossRefGoogle Scholar
  91. Woodbury NW et al (1994) Relationship between thermodynamics and mechanism during photoinduced charge separation in reaction centers from Rhodobacter Sphaeroides. Biochemistry 33:8101–8112CrossRefPubMedGoogle Scholar
  92. Youvan DC, Ismail S, Bylina EJ (1985) Chromosomal deletion and plasmid complementation of the photosynthetic reaction center and light-harvesting genes from Rhodopseudomonas capsulata. Gene 38:19–30CrossRefPubMedGoogle Scholar
  93. Zhu JY, van Stokkum IHM, Paparelli L, Jones MR, Groot ML (2013) Early bacteriopheophytin reduction in charge separation in reaction centers of Rhodobacter sphaeroides. Biophys J 104:2493–2502CrossRefPubMedPubMedCentralGoogle Scholar
  94. Zinth W, Wachtveitl J (2005) The first picoseconds in bacterial photosynthesis—ultrafast electron transfer for the efficient conversion of light energy. Chemphyschem 6:871–880CrossRefPubMedGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of ChemistryWashington UniversitySt. LouisUSA
  2. 2.Biosciences DivisionArgonne National LaboratoryLemontUSA

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