High yield of secondary B-side electron transfer in mutant Rhodobacter capsulatus reaction centers

Kressel, Lucas; Faries, Kaitlyn M.; Wander, Marc J.; Zogzas, Charles E.; Mejdrich, Rachel J.; Hanson, Deborah K.; Holten, Dewey; Laible, Philip D.; Kirmaier, Christine

doi:10.1016/j.bbabio.2014.07.015

Title: High yield of secondary B-side electron transfer in mutant Rhodobacter capsulatus reaction centers

Journal Article · Sat Nov 01 00:00:00 EDT 2014 · Biochimica et Biophysica Acta - Bioenergetics

DOI:https://doi.org/10.1016/j.bbabio.2014.07.015· OSTI ID:1225100

Kressel, Lucas; Faries, Kaitlyn M.; Wander, Marc J.;

; Mejdrich, Rachel J.; Hanson, Deborah K.; Holten, Dewey; Laible, Philip D.; Kirmaier, Christine

From the crystal structures of reaction centers (RCs) from purple photosynthetic bacteria, two pathways for electron transfer (ET) are apparent but only one pathway (the A side) operates in the native protein-cofactor complex. Partial activation of the B-side pathway has unveiled the true inefficiencies of ET processes on that side in comparison to analogous reactions on the A side. Of significance are the relative rate constants for forward ET and the competing charge recombination reactions. On the B side, these rate constants are nearly equal for the secondary charge-separation step (ET from bacteriopheophytin to quinone), relegating the yield of this process to < 50%. Herein we report efforts to optimize this step. In surveying all possible residues at position 131 in the M subunit, we discovered that when glutamic acid replaces the native valine the efficiency of the secondary ET is nearly two-fold higher than in the wild-type RC. The positive effect of M131 Glu is likely due to formation of a hydrogen bond with the ring V keto group of the B-side bacteriopheophytin leading to stabilization of the charge-separated state involving this cofactor. In conclusion, this change slows charge recombination by roughly a factor of two and affords the improved yield of the desired forward ET to the B-side quinone terminal acceptor.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG-02-09ER16116; AC02-06CH11357; FG02-09ER16116; DGE-1143954

OSTI ID:: 1225100

Alternate ID(s):: OSTI ID: 1222397; OSTI ID: 1225368

Journal Information:: Biochimica et Biophysica Acta - Bioenergetics, Journal Name: Biochimica et Biophysica Acta - Bioenergetics Vol. 1837 Journal Issue: 11; ISSN 0005-2728

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Cited by: 8 works

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References (60)

M-Side Electron Transfer in Reaction Center Mutants with a Lysine near the Nonphotoactive Bacteriochlorophyll ^† Kirmaier, Christine; Weems, Danielle; Holten, Dewey Biochemistry, Vol. 38, Issue 35 https://doi.org/10.1021/bi9908585	journal	August 1999
Determination of the Rate and Yield of B-side Quinone Reduction in Rhodobacter capsulatus Reaction Centers ^† Kee, Hooi Ling; Laible, Philip D.; Bautista, James A. Biochemistry, Vol. 45, Issue 23 https://doi.org/10.1021/bi060277x	journal	June 2006
Primary charge separation in mutant reaction centers of Rhodobacter capsulatus Jia, Yiwei; DiMagno, Theodore J.; Chan, Chi Kin The Journal of Physical Chemistry, Vol. 97, Issue 50 https://doi.org/10.1021/j100152a024	journal	December 1993
Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3Å resolution Deisenhofer, J.; Epp, O.; Miki, K. Nature, Vol. 318, Issue 6047 https://doi.org/10.1038/318618a0	journal	December 1985
Control of electron transfer between the L- and M-sides of photosynthetic reaction centers Heller, B.; Holten, D.; Kirmaier, C. Science, Vol. 269, Issue 5226 https://doi.org/10.1126/science.7638616	journal	August 1995
Insights into the factors controlling the rates of the deactivation processes that compete with charge separation in photosynthetic reaction centers Laporte, Laurent; McDowell, Lynda M.; Kirmaier, Christine Chemical Physics, Vol. 176, Issue 2-3 https://doi.org/10.1016/0301-0104(93)80265-B	journal	October 1993
Comparison of M-Side Electron Transfer in Rb. sphaeroides and Rb. capsulatus Reaction Centers Kirmaier, Christine; Laible, Philip D.; Czarnecki, Kazimierz The Journal of Physical Chemistry B, Vol. 106, Issue 7 https://doi.org/10.1021/jp013264w	journal	February 2002
Manipulations of the B-Side Charge-Separated States' Energetics in the Rhodobacter sphaeroides Reaction Center Katilius, Evaldas; Babendure, Jennie L.; Katiliene, Zivile The Journal of Physical Chemistry B, Vol. 107, Issue 43 https://doi.org/10.1021/jp035013o	journal	October 2003
Mechanism of Recombination of the P + H A – Radical Pair in Mutant Rhodobacter sphaeroides Reaction Centers with Modified Free Energy Gaps Between P + B A – and P + H A – Gibasiewicz, Krzysztof; Pajzderska, Maria; Potter, Jane A. The Journal of Physical Chemistry B, Vol. 115, Issue 44 https://doi.org/10.1021/jp206462g	journal	November 2011
Manipulating the Direction of Electron Transfer in the Bacterial Reaction Center by Swapping Phe for Tyr Near BChl _M (L181) and Tyr for Phe Near BChl _L (M208) ^† Kirmaier, Christine; He, Chunyan; Holten, Dewey Biochemistry, Vol. 40, Issue 40 https://doi.org/10.1021/bi0113263	journal	October 2001
Effects of Asp Residues Near the L-Side Pigments in Bacterial Reaction Centers ^† Heller, Barbara A.; Holten, Dewey; Kirmaier, Christine Biochemistry, Vol. 35, Issue 48 https://doi.org/10.1021/bi961362f	journal	January 1996
Effects of Hydrogen Bonds on the Redox Potential and Electronic Structure of the Bacterial Primary Electron Donor ^† Ivancich, Anabella; Artz, Katie; Williams, JoAnn C. Biochemistry, Vol. 37, Issue 34 https://doi.org/10.1021/bi9806908	journal	August 1998
A kinetic analysis of the primary charge separation in bacterial photosynthesis. Energy gaps and static heterogeneity Bixon, M.; Jortner, Joshua; Michel-Beyerle, M. E. Chemical Physics, Vol. 197, Issue 3 https://doi.org/10.1016/0301-0104(95)00168-N	journal	August 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 Kirmaier, Christine; Laporte, Laurent; Schenck, Craig C. The Journal of Physical Chemistry, Vol. 99, Issue 21 https://doi.org/10.1021/j100021a068	journal	May 1995
The Nature and Dynamics of the Charge-Separated Intermediate in Reaction Centers in which Bacteriochlorophyll Replaces the Photoactive Bacteriopheophytin. 1. Spectral Characterization of the Transient State Kirmaier, Christine; Laporte, Laurent; Schenck, Craig. C. The Journal of Physical Chemistry, Vol. 99, Issue 21 https://doi.org/10.1021/j100021a067	journal	May 1995
Electrostatic control of charge separation in bacterial photosynthesis Parson, William W.; Chu, Zhen-Tao; Warshel, Arieh Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1017, Issue 3 https://doi.org/10.1016/0005-2728(90)90192-7	journal	June 1990
P + H A - Charge Recombination Reaction Rate Constant in Rhodobacter sphaeroides Reaction Centers Is Independent of the P/P + Midpoint Potential † Tang, Chu-Kang; Williams, JoAnn C.; Taguchi, Aileen K. W. Biochemistry, Vol. 38, Issue 27 https://doi.org/10.1021/bi990346q	journal	July 1999
Fourier transform infrared study of the primary electron donor in chromatophores of Rhodobacter sphaeroides with reaction centers genetically modified at residues M160 and L131 Nabedryk, E.; Allen, J. P.; Taguchi, A. K. W. Biochemistry, Vol. 32, Issue 50 https://doi.org/10.1021/bi00213a017	journal	December 1993
Nonexponential Fluorescence Decay in Reaction Centers of Rhodobacter s phaeroides Reflecting Dispersive Charge Separation up to 1 ns † Hartwich, G.; Lossau, H.; Michel-Beyerle, M. E. The Journal of Physical Chemistry B, Vol. 102, Issue 19 https://doi.org/10.1021/jp973472h	journal	May 1998
Resonance Raman Spectroscopic Evidence for Dielectric Asymmetry in Bacterial Photosynthetic Reaction Centers Palaniappan, Vaithianathan; Bocian, David F. Journal of the American Chemical Society, Vol. 117, Issue 12 https://doi.org/10.1021/ja00117a048	journal	March 1995
Excited states of photosynthetic reaction centers at low redox potentials Parson, William W.; Clayton, Roderick K.; Cogdell, Richard J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 387, Issue 2 https://doi.org/10.1016/0005-2728(75)90109-7	journal	May 1975
Detergent effects on primary charge separation in wild-type and mutant Rhodobacter capsulatus reaction centers Kirmaier, Christine; Laible, Philip D.; Hindin, Eve Chemical Physics, Vol. 294, Issue 3 https://doi.org/10.1016/S0301-0104(03)00283-0	journal	November 2003
Electron and proton transfer to the quinones in bacterial photosynthetic reaction centers: Insight from combined approaches of molecular genetics and biophysics Sebban, P.; Maróti, P.; Hanson, D. K. Biochimie, Vol. 77, Issue 7-8 https://doi.org/10.1016/0300-9084(96)88183-1	journal	January 1995
Relationship between thermodynamics and mechanism during photoinduced charge separation in reaction centers from Rhodobacter sphaeroides. Woodbury, Neal W.; Peloquin, Jeffrey M.; Alden, Rhett G. Biochemistry, Vol. 33, Issue 26 https://doi.org/10.1021/bi00192a015	journal	July 1994
Relationship between the oxidation potential of the bacteriochlorophyll dimer and electron transfer in photosynthetic reaction centers Allen, J. P.; Williams, J. C. Journal of Bioenergetics and Biomembranes, Vol. 27, Issue 3 https://doi.org/10.1007/BF02110097	journal	June 1995
Influence of an amino-acid residue on the optical properties and electron transfer dynamics of a photosynthetic reaction centre complex Bylina, Edward J.; Kirmaier, Christine; McDowell, Lynda Nature, Vol. 336, Issue 6195 https://doi.org/10.1038/336182a0	journal	November 1988
Trapped Conformational States of Semiquinone (D ⁺ ^• Q _B ^- ^• ) Formed by B-Branch Electron Transfer at Low Temperature in Rhodobacter sphaeroides Reaction Centers ^† Paddock, M. L.; Flores, M.; Isaacson, R. Biochemistry, Vol. 45, Issue 47 https://doi.org/10.1021/bi060854h	journal	November 2006
Formation of a Semiquinone at the Q _B Site by A- or B-Branch Electron Transfer in the Reaction Center from Rhodobacter sphaeroides ^† Wakeham, Marion C.; Breton, Jacques; Nabedryk, Eliane Biochemistry, Vol. 43, Issue 16 https://doi.org/10.1021/bi035726x	journal	April 2004
Quinone Reduction via Secondary B-Branch Electron Transfer in Mutant Bacterial Reaction Centers ^† Laible, Philip D.; Kirmaier, Christine; Udawatte, Chandani S. M. Biochemistry, Vol. 42, Issue 6 https://doi.org/10.1021/bi026959b	journal	February 2003
Unidirectionality of charge separation in reaction centers of photosynthetic bacteria Michel-Beyerle, M. E.; Plato, M.; Deisenhofer, J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 932 https://doi.org/10.1016/0005-2728(88)90139-9	journal	January 1988
Energetics and Kinetics of Radical Pairs in Reaction Centers from Rhodobacter sphaeroides . A Femtosecond Transient Absorption Study ^† ^, ^‡ Holzwarth, A. R.; Müller, Marc G. Biochemistry, Vol. 35, Issue 36 https://doi.org/10.1021/bi9607012	journal	January 1996
Analysis of the temperature-dependence of P+HA− charge recombination in the Rhodobacter sphaeroides reaction center suggests nanosecond temperature-independent protein relaxation Gibasiewicz, Krzysztof; Pajzderska, Maria; Dobek, Andrzej Physical Chemistry Chemical Physics, Vol. 15, Issue 38 https://doi.org/10.1039/c3cp44187c	journal	January 2013
Putative Hydrogen Bond to Tyrosine M208 in Photosynthetic Reaction Centers from Rhodobacter capsulatus Significantly Slows Primary Charge Separation Saggu, Miguel; Carter, Brett; Zhou, Xiaoxue The Journal of Physical Chemistry B, Vol. 118, Issue 24 https://doi.org/10.1021/jp503422c	journal	June 2014
Characterization of the bonding interactions of QB upon photoreduction via A-branch or B-branch electron transfer in mutant reaction centers from Rhodobacter sphaeroides Breton, Jacques; Wakeham, Marion C.; Fyfe, Paul K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1656, Issue 2-3 https://doi.org/10.1016/j.bbabio.2004.02.005	journal	June 2004
Atavistic reaction centre Coleman, William J.; Youvan, Douglas C. Nature, Vol. 366, Issue 6455 https://doi.org/10.1038/366517a0	journal	December 1993
Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors. Allen, J. P.; Feher, G.; Yeates, T. O. Proceedings of the National Academy of Sciences, Vol. 84, Issue 16 https://doi.org/10.1073/pnas.84.16.5730	journal	August 1987
Orientation of the OH Dipole of Tyrosine (M)210 and Its Effect on Electrostatic Energies in Photosynthetic Bacterial Reaction Centers Alden, Rhett G.; Parson, William W.; Chu, Zhen Tao The Journal of Physical Chemistry, Vol. 100, Issue 41 https://doi.org/10.1021/jp961271s	journal	January 1996
High Yield of M-Side Electron Transfer in Mutants of Rhodobacter capsulatus Reaction Centers Lacking the L-Side Bacteriopheophytin ^† Chuang, Jessica I.; Boxer, Steven G.; Holten, Dewey Biochemistry, Vol. 45, Issue 12 https://doi.org/10.1021/bi0601048	journal	March 2006
High Throughput Engineering to Revitalize a Vestigial Electron Transfer Pathway in Bacterial Photosynthetic Reaction Centers Faries, Kaitlyn M.; Kressel, Lucas L.; Wander, Marc J. Journal of Biological Chemistry, Vol. 287, Issue 11 https://doi.org/10.1074/jbc.M111.326447	journal	January 2012
B-Side Electron Transfer To Form P ⁺ H _B ^- in Reaction Centers from the F(L181)Y/Y(M208)F Mutant of Rhodobacter c apsulatus Kirmaier, Christine; Laible, Philip D.; Hanson, Deborah K. The Journal of Physical Chemistry B, Vol. 108, Issue 31 https://doi.org/10.1021/jp0485441	journal	August 2004
Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin Kirmaier, C.; Gaul, D.; DeBey, R. Science, Vol. 251, Issue 4996 https://doi.org/10.1126/science.2000491	journal	February 1991
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 Kakitani, Yoshinori; Hou, Ali; Miyasako, Yuya Chemical Physics Letters, Vol. 492, Issue 1-3 https://doi.org/10.1016/j.cplett.2010.03.071	journal	May 2010
Investigation of B-branch electron transfer by femtosecond time resolved spectroscopy in a Rhodobacter sphaeroides reaction centre that lacks the QA ubiquinone Frolov, Dmitrij; Wakeham, Marion C.; Andrizhiyevskaya, Elena G. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1707, Issue 2-3 https://doi.org/10.1016/j.bbabio.2004.12.006	journal	April 2005
Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides Woodbury, Neal W. T.; Parson, William W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 767, Issue 2 https://doi.org/10.1016/0005-2728(84)90205-6	journal	November 1984
Quinone (Q _B ) Reduction by B-Branch Electron Transfer in Mutant Bacterial Reaction Centers from Rhodobacter sphaeroides : Quantum Efficiency and X-ray Structure ^† ^, ^‡ Paddock, M. L.; Chang, C.; Xu, Q. Biochemistry, Vol. 44, Issue 18 https://doi.org/10.1021/bi047559m	journal	May 2005
Triplet states of bacteriochlorophyll and carotenoids in chromatophores of photosynthetic bacteria Monger, Teresa G.; Cogdell, Richard J.; Parson, William W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 449, Issue 1 https://doi.org/10.1016/0005-2728(76)90013-X	journal	October 1976
B-Side Charge Separation in Bacterial Photosynthetic Reaction Centers: Nanosecond Time Scale Electron Transfer from H _B ^- to Q _B ^† Kirmaier, Christine; Laible, Philip D.; Hanson, Deborah K. Biochemistry, Vol. 42, Issue 7 https://doi.org/10.1021/bi026973o	journal	February 2003
Photo-accumulation of the P ⁺ Q _B ⁻ radical pair state in purple bacterial reaction centres that lack the Q _A ubiquinone Wakeham, Marion C.; Goodwin, Matthew G.; McKibbin, Craig FEBS Letters, Vol. 540, Issue 1-3 https://doi.org/10.1016/S0014-5793(03)00270-9	journal	March 2003
Probing M-Branch Electron Transfer and Cofactor Environment in the Bacterial Photosynthetic Reaction Center by Addition of a Hydrogen Bond to the M-Side Bacteriopheophytin Kirmaier, Christine; Cua, Agnes; He, Chunyan The Journal of Physical Chemistry B, Vol. 106, Issue 2 https://doi.org/10.1021/jp012768r	journal	January 2002
B-Side Electron Transfer in a Rhodobacter sphaeroides Reaction Center Mutant in Which the B-Side Monomer Bacteriochlorophyll Is Replaced with Bacteriopheophytin Katilius, Evaldas; Turanchik, Trieva; Lin, Su The Journal of Physical Chemistry B, Vol. 103, Issue 35 https://doi.org/10.1021/jp991670y	journal	September 1999
Electrostatic Potentials in Rhodopseudomonas viridis Reaction Centers: Implications for the Driving Force and Directionality of Electron Transfer ^† Gunner, M. R.; Nicholls, Anthony; Honig, Barry The Journal of Physical Chemistry, Vol. 100, Issue 10 https://doi.org/10.1021/jp9519070	journal	January 1996
Delayed fluorescence from Rhodopseudomonas sphaeroides reaction centers. Enthalpy and free energy changes accompanying electron transfer from P-870 to quinones Arata, Hiroyuki; Parson, William W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 638, Issue 2 https://doi.org/10.1016/0005-2728(81)90228-0	journal	December 1981
Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2.65 å resolution: cofactors and protein-cofactor interactions Ermler, Ulrich; Fritzsch, Günter; Buchanan, Susan K. Structure, Vol. 2, Issue 10 https://doi.org/10.1016/S0969-2126(94)00094-8	journal	October 1994
The First Picoseconds in Bacterial Photosynthesis?Ultrafast Electron Transfer for the Efficient Conversion of Light Energy Zinth, Wolfgang; Wachtveitl, Josef ChemPhysChem, Vol. 6, Issue 5 https://doi.org/10.1002/cphc.200400458	journal	May 2005
Trapping the P ⁺ B _L ⁻ Initial Intermediate State of Charge Separation in Photosynthetic Reaction Centers from Rhodobacter capsulatus Carter, Brett; Boxer, Steven G.; Holten, Dewey Biochemistry, Vol. 48, Issue 12 https://doi.org/10.1021/bi900282p	journal	February 2009
Rewiring photosynthesis: engineering wrong-way electron transfer in the purple bacterial reaction centre Wakeham, M. C.; Jones, M. R. Biochemical Society Transactions, Vol. 33, Issue 4 https://doi.org/10.1042/BST0330851	journal	August 2005
A Conformational Change of the Photoactive Bacteriopheophytin in Reaction Centers from Rhodobacter sphaeroides ^† Müh, Frank; Williams, JoAnn C.; Allen, James P. Biochemistry, Vol. 37, Issue 38 https://doi.org/10.1021/bi980799f	journal	September 1998
The accessory bacteriochlorophyll: a real electron carrier in primary photosynthesis. Arlt, T.; Schmidt, S.; Kaiser, W. Proceedings of the National Academy of Sciences, Vol. 90, Issue 24 https://doi.org/10.1073/pnas.90.24.11757	journal	December 1993
Photochemistry of a Bacterial Photosynthetic Reaction Center Missing the Initial Bacteriochlorophyll Electron Acceptor Carter, Brett; Boxer, Steven G.; Holten, Dewey The Journal of Physical Chemistry B, Vol. 116, Issue 33 https://doi.org/10.1021/jp305276m	journal	August 2012
Temperature Dependence of Electron Transfer to the M-Side Bacteriopheophytin in Rhodobacter capsulatus Reaction Centers Chuang, Jessica I.; Boxer, Steven G.; Holten, Dewey The Journal of Physical Chemistry B, Vol. 112, Issue 17 https://doi.org/10.1021/jp800082m	journal	May 2008

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Title: High yield of secondary B-side electron transfer in mutant Rhodobacter capsulatus reaction centers

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