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Title: Redox potential tuning through differential quinone binding in the photosynthetic reaction center of Rhodobacter sphaeroides

Abstract

Ubiquinone forms an integral part of the electron transport chain in cellular respiration and photosynthesis across a vast number of organisms. Prior experimental results have shown that the photosynthetic reaction center (RC) from Rhodobacter sphaeroides is only fully functional with a limited set of methoxy-bearing quinones, suggesting that specific interactions with this substituent are required to drive electron transport and the formation of quinol. The nature of these interactions has yet to be determined. Through parameterization of a CHARMM-compatible quinone force field and subsequent molecular dynamics simulations of the quinone-bound RC, in this paper we have investigated and characterized the interactions of the protein with the quinones in the QA and QB sites using both equilibrium simulation and thermodynamic integration. In particular, we identify a specific interaction between the 2-methoxy group of ubiquinone in the QB site and the amide nitrogen of GlyL225 that we implicate in locking the orientation of the 2-methoxy group, thereby tuning the redox potential difference between the quinones occupying the QA and QB sites. Finally, disruption of this interaction leads to weaker binding in a ubiquinone analogue that lacks a 2-methoxy group, a finding supported by reverse electron transfer electron paramagnetic resonance experiments of themore » QA–QB– biradical and competitive binding assays.« less

Authors:
 [1];  [1];  [1];  [1];  [1]
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  1. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
Publication Date:
Research Org.:
Univ. of Illinois at Urbana-Champaign, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1344901
Grant/Contract Number:  
FG02-97ER25308; FG02-08ER15960; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 54; Journal Issue: 12; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Vermaas, Josh V., Taguchi, Alexander T., Dikanov, Sergei A., Wraight, Colin A., and Tajkhorshid, Emad. Redox potential tuning through differential quinone binding in the photosynthetic reaction center of Rhodobacter sphaeroides. United States: N. p., 2015. Web. doi:10.1021/acs.biochem.5b00033.
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Vermaas, Josh V., Taguchi, Alexander T., Dikanov, Sergei A., Wraight, Colin A., & Tajkhorshid, Emad. Redox potential tuning through differential quinone binding in the photosynthetic reaction center of Rhodobacter sphaeroides. United States. https://doi.org/10.1021/acs.biochem.5b00033
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Vermaas, Josh V., Taguchi, Alexander T., Dikanov, Sergei A., Wraight, Colin A., and Tajkhorshid, Emad. Tue . "Redox potential tuning through differential quinone binding in the photosynthetic reaction center of Rhodobacter sphaeroides". United States. https://doi.org/10.1021/acs.biochem.5b00033. https://www.osti.gov/servlets/purl/1344901.
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@article{osti_1344901,
title = {Redox potential tuning through differential quinone binding in the photosynthetic reaction center of Rhodobacter sphaeroides},
author = {Vermaas, Josh V. and Taguchi, Alexander T. and Dikanov, Sergei A. and Wraight, Colin A. and Tajkhorshid, Emad},
abstractNote = {Ubiquinone forms an integral part of the electron transport chain in cellular respiration and photosynthesis across a vast number of organisms. Prior experimental results have shown that the photosynthetic reaction center (RC) from Rhodobacter sphaeroides is only fully functional with a limited set of methoxy-bearing quinones, suggesting that specific interactions with this substituent are required to drive electron transport and the formation of quinol. The nature of these interactions has yet to be determined. Through parameterization of a CHARMM-compatible quinone force field and subsequent molecular dynamics simulations of the quinone-bound RC, in this paper we have investigated and characterized the interactions of the protein with the quinones in the QA and QB sites using both equilibrium simulation and thermodynamic integration. In particular, we identify a specific interaction between the 2-methoxy group of ubiquinone in the QB site and the amide nitrogen of GlyL225 that we implicate in locking the orientation of the 2-methoxy group, thereby tuning the redox potential difference between the quinones occupying the QA and QB sites. Finally, disruption of this interaction leads to weaker binding in a ubiquinone analogue that lacks a 2-methoxy group, a finding supported by reverse electron transfer electron paramagnetic resonance experiments of the QA–QB– biradical and competitive binding assays.},
doi = {10.1021/acs.biochem.5b00033},
journal = {Biochemistry},
number = 12,
volume = 54,
place = {United States},
year = {Tue Mar 03 00:00:00 EST 2015},
month = {Tue Mar 03 00:00:00 EST 2015}
}
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https://doi.org/10.1021/acs.biochem.5b00033
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Works referenced in this record:

Proton and electron transfer in bacterial reaction centers
journal, May 2000

  • Okamura, M. Y.; Paddock, M. L.; Graige, M. S.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1458, Issue 1
  • DOI: 10.1016/S0005-2728(00)00065-7

Electron acceptors of bacterial photosynthetic reaction centers II. H+ binding coupled to secondary electron transfer in the quinone acceptor complex
journal, November 1979

Electrochemistry of ubiquinones: Menaquinones and plastoquinones in aprotic solvents
journal, August 1983

Structure of the reaction center from Rhodobacter sphaeroides R-26: the cofactors.
journal, August 1987

  • Allen, J. P.; Feher, G.; Yeates, T. O.
  • Proceedings of the National Academy of Sciences, Vol. 84, Issue 16
  • DOI: 10.1073/pnas.84.16.5730

Photosynthesis
book, January 2001

The 2-Methoxy Group Orientation Regulates the Redox Potential Difference between the Primary (QA) and Secondary (QB) Quinones of Type II Bacterial Photosynthetic Reaction Centers
journal, July 2014

  • de Almeida, Wagner B.; Taguchi, Alexander T.; Dikanov, Sergei A.
  • The Journal of Physical Chemistry Letters, Vol. 5, Issue 15
  • DOI: 10.1021/jz500967d

Affinity and activity of non-native quinones at the QB site of bacterial photosynthetic reaction centers
journal, May 2013

The 2-methoxy group of ubiquinone is essential for function of the acceptor quinones in reaction centers from Rba. sphaeroides
journal, July 2008

  • Wraight, Colin A.; Vakkasoglu, Ahmet S.; Poluektov, Yuri
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 7-8
  • DOI: 10.1016/j.bbabio.2008.04.025

Anab initio force field for the cofactors of bacterial photosynthesis
journal, January 2002

  • Ceccarelli, Matteo; Procacci, Piero; Marchi, Massimo
  • Journal of Computational Chemistry, Vol. 24, Issue 2
  • DOI: 10.1002/jcc.10198

Excitons in a photosynthetic light-harvesting system: A combined molecular dynamics, quantum chemistry, and polaron model study
journal, March 2002

Comparison of Secondary Structure Formation Using 10 Different Force Fields in Microsecond Molecular Dynamics Simulations
journal, July 2012

  • Cino, Elio A.; Choy, Wing-Yiu; Karttunen, Mikko
  • Journal of Chemical Theory and Computation, Vol. 8, Issue 8
  • DOI: 10.1021/ct300323g

Rapid parameterization of small molecules using the force field toolkit
journal, September 2013

  • Mayne, Christopher G.; Saam, Jan; Schulten, Klaus
  • Journal of Computational Chemistry, Vol. 34, Issue 32
  • DOI: 10.1002/jcc.23422

Determination of the binding sites of the proton transfer inhibitors Cd2+ and Zn2+ in bacterial reaction centers
journal, February 2000

  • Axelrod, H. L.; Abresch, E. C.; Paddock, M. L.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 4
  • DOI: 10.1073/pnas.97.4.1542

pH Modulates the Quinone Position in the Photosynthetic Reaction Center from Rhodobacter sphaeroides in the Neutral and Charge Separated States
journal, August 2007

  • Koepke, Juergen; Krammer, Eva-Maria; Klingen, Astrid R.
  • Journal of Molecular Biology, Vol. 371, Issue 2
  • DOI: 10.1016/j.jmb.2007.04.082

Scalable molecular dynamics with NAMD
journal, January 2005

  • Phillips, James C.; Braun, Rosemary; Wang, Wei
  • Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
  • DOI: 10.1002/jcc.20289

Optimization of the Additive CHARMM All-Atom Protein Force Field Targeting Improved Sampling of the Backbone ϕ, ψ and Side-Chain χ 1 and χ 2 Dihedral Angles
journal, August 2012

  • Best, Robert B.; Zhu, Xiao; Shim, Jihyun
  • Journal of Chemical Theory and Computation, Vol. 8, Issue 9
  • DOI: 10.1021/ct300400x

Empirical force fields for biological macromolecules: Overview and issues
journal, January 2004

  • Mackerell, Alexander D.
  • Journal of Computational Chemistry, Vol. 25, Issue 13
  • DOI: 10.1002/jcc.20082

All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins †
journal, April 1998

  • MacKerell, A. D.; Bashford, D.; Bellott, M.
  • The Journal of Physical Chemistry B, Vol. 102, Issue 18
  • DOI: 10.1021/jp973084f

Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types
journal, June 2010

  • Klauda, Jeffery B.; Venable, Richard M.; Freites, J. Alfredo
  • The Journal of Physical Chemistry B, Vol. 114, Issue 23
  • DOI: 10.1021/jp101759q

Comparison of simple potential functions for simulating liquid water
journal, July 1983

  • Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
  • The Journal of Chemical Physics, Vol. 79, Issue 2
  • DOI: 10.1063/1.445869

Classical force field parameters for the heme prosthetic group of cytochrome c
journal, October 2004

  • Autenrieth, Felix; Tajkhorshid, Emad; Baudry, Jerome
  • Journal of Computational Chemistry, Vol. 25, Issue 13
  • DOI: 10.1002/jcc.20079

Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993

  • Darden, Tom; York, Darrin; Pedersen, Lee
  • The Journal of Chemical Physics, Vol. 98, Issue 12
  • DOI: 10.1063/1.464397

A smooth particle mesh Ewald method
journal, November 1995

  • Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L.
  • The Journal of Chemical Physics, Vol. 103, Issue 19
  • DOI: 10.1063/1.470117

Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models
journal, October 1992

  • Miyamoto, Shuichi; Kollman, Peter A.
  • Journal of Computational Chemistry, Vol. 13, Issue 8
  • DOI: 10.1002/jcc.540130805

Constant pressure molecular dynamics algorithms
journal, September 1994

  • Martyna, Glenn J.; Tobias, Douglas J.; Klein, Michael L.
  • The Journal of Chemical Physics, Vol. 101, Issue 5
  • DOI: 10.1063/1.467468

Constant pressure molecular dynamics simulation: The Langevin piston method
journal, September 1995

  • Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W.
  • The Journal of Chemical Physics, Vol. 103, Issue 11
  • DOI: 10.1063/1.470648

VMD: Visual molecular dynamics
journal, February 1996

Molecular dynamics simulations of ubiquinone; a survey over torsional potentials and hydrogen bonds
journal, November 2001

  • Nilsson, J. Arvid; Lyubartsev, Alexander; Eriksson, Leif A.
  • Molecular Physics, Vol. 99, Issue 21
  • DOI: 10.1080/00268970110072403

The site-directed mutation I(L177)H in Rhodobacter sphaeroides reaction center affects coordination of PA and BB bacteriochlorophylls
journal, August 2012

  • Vasilieva, L. G.; Fufina, T. Y.; Gabdulkhakov, A. G.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8
  • DOI: 10.1016/j.bbabio.2012.02.008

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 –
journal, November 2011

  • Gibasiewicz, Krzysztof; Pajzderska, Maria; Potter, Jane A.
  • The Journal of Physical Chemistry B, Vol. 115, Issue 44
  • DOI: 10.1021/jp206462g

Importance of the Conformation of Methoxy Groups on the Vibrational and Electrochemical Properties of Ubiquinones
journal, August 1997

  • Burie, Jean-René; Boullais, Claude; Nonella, Marco
  • The Journal of Physical Chemistry B, Vol. 101, Issue 33
  • DOI: 10.1021/jp970640x

Car-Parrinello molecular dynamics simulations and EPR property calculations on aqueous ubisemiquinone radical anion
journal, January 2008

Site-specific isotope labeling demonstrates a large mesomeric resonance effect of the methoxy groups on the carbonyl frequency in ubiquinones
journal, March 1998

  • Boullais, Claude; Nabedryk, Eliane; Burie, Jean-René
  • Photosynthesis Research, Vol. 55, Issue 2/3, p. 247-252
  • DOI: 10.1023/A:1005979817422

High‐Temperature Equation of State by a Perturbation Method. I. Nonpolar Gases
journal, August 1954

  • Zwanzig, Robert W.
  • The Journal of Chemical Physics, Vol. 22, Issue 8
  • DOI: 10.1063/1.1740409

Partition coefficients of quinones and hydroquinones and their relation to biochemical reactivity
journal, August 1990

A Toolkit for the Analysis of Free-Energy Perturbation Calculations
journal, July 2012

  • Liu, Peng; Dehez, François; Cai, Wensheng
  • Journal of Chemical Theory and Computation, Vol. 8, Issue 8
  • DOI: 10.1021/ct300242f

Efficient estimation of free energy differences from Monte Carlo data
journal, October 1976

Matplotlib: A 2D Graphics Environment
journal, January 2007

Statistical Mechanics of Fluid Mixtures
journal, May 1935

  • Kirkwood, John G.
  • The Journal of Chemical Physics, Vol. 3, Issue 5
  • DOI: 10.1063/1.1749657

Free energy calculations: Applications to chemical and biochemical phenomena
journal, November 1993

Improved convergence in dual-topology free energy calculations through use of harmonic restraints
journal, August 1998

Computations of Standard Binding Free Energies with Molecular Dynamics Simulations
journal, February 2009

  • Deng, Yuqing; Roux, Benoît
  • The Journal of Physical Chemistry B, Vol. 113, Issue 8
  • DOI: 10.1021/jp807701h

Soft-core potentials in thermodynamic integration: Comparing one- and two-step transformations
journal, August 2011

  • Steinbrecher, Thomas; Joung, InSuk; Case, David A.
  • Journal of Computational Chemistry, Vol. 32, Issue 15
  • DOI: 10.1002/jcc.21909

Rapid isolation of bacterial photosynthetic reaction centers with an engineered poly-histidine tag
journal, September 1996

  • Goldsmith, Joshua O.; Boxer, Steven G.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1276, Issue 3
  • DOI: 10.1016/0005-2728(96)00091-6

Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides.
journal, September 1975

  • Okamura, M. Y.; Isaacson, R. A.; Feher, G.
  • Proceedings of the National Academy of Sciences, Vol. 72, Issue 9
  • DOI: 10.1073/pnas.72.9.3491

EPR Study of the Molecular and Electronic Structure of the Semiquinone Biradical QA-•QB-•in Photosynthetic Reaction Centers fromRhodobactersphaeroides
journal, July 2000

  • Calvo, Rafael; Abresch, Edward C.; Bittl, Robert
  • Journal of the American Chemical Society, Vol. 122, Issue 30
  • DOI: 10.1021/ja000399r

Prediction of the n -hexane/water and 1-octanol/water partition coefficients for environmentally relevant compounds using molecular simulation
journal, August 2011

  • Garrido, Nuno M.; Economou, Ioannis G.; Queimada, António J.
  • AIChE Journal, Vol. 58, Issue 6
  • DOI: 10.1002/aic.12718

Solubility of Organic Compounds in Water/Octanol Systems. A Expanded Ensemble Molecular Dynamics Simulation Study of log P Parameters
journal, August 2001

  • Lyubartsev, Alexander P.; Jacobsson, Sven P.; Sundholm, Göran
  • The Journal of Physical Chemistry B, Vol. 105, Issue 32
  • DOI: 10.1021/jp0036902

Hyperfine and Nuclear Quadrupole Tensors of Nitrogen Donors in the Q A Site of Bacterial Reaction Centers: Correlation of the Histidine N δ Tensors with Hydrogen Bond Strength
journal, July 2014

  • Taguchi, Alexander T.; O’Malley, Patrick J.; Wraight, Colin A.
  • The Journal of Physical Chemistry B, Vol. 118, Issue 31
  • DOI: 10.1021/jp5051029

Hydrogen Bonds between Nitrogen Donors and the Semiquinone in the Q B Site of Bacterial Reaction Centers
journal, August 2010

  • Martin, Erik; Samoilova, Rimma I.; Narasimhulu, Kupala V.
  • Journal of the American Chemical Society, Vol. 132, Issue 33
  • DOI: 10.1021/ja104134e

Hydrogen Bonding and Spin Density Distribution in the Q B Semiquinone of Bacterial Reaction Centers and Comparison with the Q A Site
journal, April 2011

  • Martin, Erik; Samoilova, Rimma I.; Narasimhulu, Kupala V.
  • Journal of the American Chemical Society, Vol. 133, Issue 14
  • DOI: 10.1021/ja2001538

On the Nature of the Hydrogen Bonds to Neutral Ubiquinone in the Q A Binding Site in Purple Bacterial Photosynthetic Reaction Centers
journal, July 2013

  • Zhao, Nan; Hastings, Gary
  • The Journal of Physical Chemistry B, Vol. 117, Issue 29
  • DOI: 10.1021/jp403833y

Variation of Ser-L223 Hydrogen Bonding with the QB Redox State in Reaction Centers from Rhodobacter sphaeroides
journal, June 2004

  • Ishikita, Hiroshi; Knapp, Ernst-Walter
  • Journal of the American Chemical Society, Vol. 126, Issue 25
  • DOI: 10.1021/ja038092q

Hydrogen Bonding between the Q B Site Ubisemiquinone and Ser-L223 in the Bacterial Reaction Center: A Combined Spectroscopic and Computational Perspective
journal, October 2012

  • Martin, Erik; Baldansuren, Amgalanbaatar; Lin, Tzu-Jen
  • Biochemistry, Vol. 51, Issue 45
  • DOI: 10.1021/bi300834w
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    Works referencing / citing this record:

    Partition, orientation and mobility of ubiquinones in a lipid bilayer
    journal, December 2015

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    • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 12
    • DOI: 10.1016/j.bbabio.2015.08.001
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