Electrostatic Influence on Photoisomerization in Bacteriorhodopsin and Halorhodopsin

Punwong, Chutintorn; Hannongbua, Supot; Martínez, Todd J.

doi:10.1021/acs.jpcb.9b01837

Electrostatic Influence on Photoisomerization in Bacteriorhodopsin and Halorhodopsin

Journal Article · Wed May 22 00:00:00 EDT 2019 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.9b01837· OSTI ID:1547066

^[1]; Hannongbua, Supot ^[2]; ^[3]

Prince of Songkla Univ. (Thailand)
Chulalongkorn Univ., Bangkok (Thailand)
Stanford Univ., CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)

Bacteriorhodopsin (bR) and halorhodopsin (hR) are mutual membrane proteins that transport ions across the cell membrane in halobacteria. Their ion transport function is triggered by photoactivated isomerization of the retinal protonated Schiff base (RPSB) chromophore. In spite of their similar structures, bR and hR exhibit widely differing RPSB isomerization rates and quantum yields (with bR being both faster and more efficient than hR). Previous simulations of photoisomerization in bR and hR using ab initio multiple spawning (AIMS) with QM/MM have successfully reproduced the experimentally observed ordering of quantum yields and isomerization rates, but the origin of these differences remains elusive. In this work, we discover the role of electrostatic interactions in the protein pocket surrounding RPSB. We probe the influence of protein electrostatics by modifying the charge of the complex counterion in bR/hR to be more/less negative than the native state. We find that such modifications lead to bR-like behavior in hR and vice versa. This demonstrates the crucial role of electrostatic interactions in controlling the outcome of RPSB photoisomerization.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE; National Science Foundation (NSF); Thailand Research Fund

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1547066

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Journal Name: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry Journal Issue: 23 Vol. 123; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Ab Initio Quantum Molecular Dynamics Ben-Nun, Michal; Martínez, Todd. J. Advances in Chemical Physics, Volume 121 https://doi.org/10.1002/0471264318.ch7	book	January 2002
QM/MM Methods for Biomolecular Systems Senn, Hans Martin; Thiel, Walter Angewandte Chemie International Edition, Vol. 48, Issue 7 https://doi.org/10.1002/anie.200802019	journal	January 2009
The photocycle of the chloride pump halorhodopsin. II: Quantum yields and a kinetic model Oesterhelt, D.; Hegemann, P.; Tittor, J. The EMBO Journal, Vol. 4, Issue 9 https://doi.org/10.1002/j.1460-2075.1985.tb03938.x	journal	September 1985
Combined QM/MM study of the opsin shift in bacteriorhodopsin Rajamani, Ramkumar; Gao, Jiali Journal of Computational Chemistry, Vol. 23, Issue 1 https://doi.org/10.1002/jcc.1159	journal	November 2001
General atomic and molecular electronic structure system Schmidt, Michael W.; Baldridge, Kim K.; Boatz, Jerry A. Journal of Computational Chemistry, Vol. 14, Issue 11, p. 1347-1363 https://doi.org/10.1002/jcc.540141112	journal	November 1993
Structure of bacteriorhodopsin at 1.55 Å resolution Luecke, Hartmut; Schobert, Brigitte; Richter, Hans-Thomas Journal of Molecular Biology, Vol. 291, Issue 4 https://doi.org/10.1006/jmbi.1999.3027	journal	August 1999
An Introduction to the Bootstrap Efron, Bradley; Tibshirani, Robert J. Chapman and Hall/CRC https://doi.org/10.1007/978-1-4899-4541-9	book	January 1993
QM/MM connection atoms for the multistate treatment of organic and biological molecules Toniolo, A.; Ciminelli, C.; Granucci, G. Theoretical Chemistry Accounts, Vol. 111, Issue 2-6 https://doi.org/10.1007/s00214-003-0522-7	journal	December 2003
Femtosecond absorption spectroscopy of light-adapted and dark-adapted bacteriorhodopsin Petrich, J. W.; Breton, J.; Martin, J. L. Chemical Physics Letters, Vol. 137, Issue 4 https://doi.org/10.1016/0009-2614(87)80902-8	journal	June 1987
Excited-state reaction dynamics of bacteriorhodopsin studied by femtosecond spectroscopy Dobler, J.; Zinth, W.; Kaiser, W. Chemical Physics Letters, Vol. 144, Issue 2 https://doi.org/10.1016/0009-2614(88)87120-3	journal	February 1988
The initial reaction dynamics of the light-driven chloride pump halorhodopsin Arlt, T.; Schmidt, S.; Zinth, W. Chemical Physics Letters, Vol. 241, Issue 5-6 https://doi.org/10.1016/0009-2614(95)00664-P	journal	August 1995
The quantum yield of bacteriorhodopsin Tittor, Jörg; Oesterhelt, Dieter FEBS Letters, Vol. 263, Issue 2 https://doi.org/10.1016/0014-5793(90)81390-A	journal	April 1990
Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling Torrie, G. M.; Valleau, J. P. Journal of Computational Physics, Vol. 23, Issue 2 https://doi.org/10.1016/0021-9991(77)90121-8	journal	February 1977
Theoretical studies of enzymic reactions: Dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme Warshel, A.; Levitt, M. Journal of Molecular Biology, Vol. 103, Issue 2 https://doi.org/10.1016/0022-2836(76)90311-9	journal	May 1976
Functional interactions in bacteriorhodopsin: a theoretical analysis of retinal hydrogen bonding with water Nina, M.; Roux, B.; Smith, J. C. Biophysical Journal, Vol. 68, Issue 1 https://doi.org/10.1016/S0006-3495(95)80184-0	journal	January 1995
Molecular gradients for semiempirical CI wavefunctions with floating occupation molecular orbitals Granucci, Giovanni; Toniolo, Alessandro Chemical Physics Letters, Vol. 325, Issue 1-3 https://doi.org/10.1016/S0009-2614(00)00691-6	journal	July 2000
Characterization of a conical intersection between the ground and first excited state for a retinal analog Molnar, F.; Ben-Nun, M.; Martı́nez, T. J. Journal of Molecular Structure: THEOCHEM, Vol. 506, Issue 1-3 https://doi.org/10.1016/S0166-1280(00)00410-3	journal	July 2000
Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 Å resolution Belrhali, Hassan; Nollert, Peter; Royant, Antoine Structure, Vol. 7, Issue 8 https://doi.org/10.1016/S0969-2126(99)80118-X	journal	August 1999
Excited state direct dynamics of benzene with reparameterized multi-reference semiempirical configuration interaction methods Toniolo, A.; Thompson, Alexis L.; Martı́nez, Todd J. Chemical Physics, Vol. 304, Issue 1-2 https://doi.org/10.1016/j.chemphys.2004.04.018	journal	September 2004
Primary reaction dynamics of halorhodopsin, observed by sub-picosecond IR – vibrational spectroscopy Peters, Frank; Herbst, Johannes; Tittor, Jörg Chemical Physics, Vol. 323, Issue 1 https://doi.org/10.1016/j.chemphys.2005.08.036	journal	March 2006
Implementation of ab initio multiple spawning in the Molpro quantum chemistry package Levine, Benjamin G.; Coe, Joshua D.; Virshup, Aaron M. Chemical Physics, Vol. 347, Issue 1-3 https://doi.org/10.1016/j.chemphys.2008.01.014	journal	May 2008
Direct QM/MM simulation of photoexcitation dynamics in bacteriorhodopsin and halorhodopsin Punwong, C.; Martínez, T. J.; Hannongbua, S. Chemical Physics Letters, Vol. 610-611 https://doi.org/10.1016/j.cplett.2014.07.037	journal	August 2014
Ab Initio Nonadiabatic Quantum Molecular Dynamics Curchod, Basile F. E.; Martínez, Todd J. Chemical Reviews, Vol. 118, Issue 7 https://doi.org/10.1021/acs.chemrev.7b00423	journal	February 2018
Insights for Light-Driven Molecular Devices from Ab Initio Multiple Spawning Excited-State Dynamics of Organic and Biological Chromophores Martínez, Todd J. Accounts of Chemical Research, Vol. 39, Issue 2 https://doi.org/10.1021/ar040202q	journal	February 2006
Theoretical Studies of Electronically Excited States of Molecular Systems Using Multiconfigurational Perturbation Theory Roos, Björn O. Accounts of Chemical Research, Vol. 32, Issue 2 https://doi.org/10.1021/ar960091y	journal	February 1999
The Complex Extracellular Domain Regulates the Deprotonation and Reprotonation of the Retinal Schiff Base during the Bacteriorhodopsin Photocycle Brown, Leonid S.; Varo, Gyoergy; Hatanaka, Minoru Biochemistry, Vol. 34, Issue 39 https://doi.org/10.1021/bi00039a053	journal	October 1995
Complete Identification of C:O Stretching Vibrational Bands of Protonated Aspartic Acid Residues in the Difference Infrared Spectra of M and N Intermediates versus Bacteriorhodopsin Sasaki, Jun; Lanyi, Janos K.; Needleman, Richard Biochemistry, Vol. 33, Issue 11 https://doi.org/10.1021/bi00177a006	journal	March 1994
Vibrational Frequency and Dipolar Orientation of the Protonated Schiff Base in Bacteriorhodopsin before and after Photoisomerization ^† Kandori, Hideki; Belenky, Marina; Herzfeld, Judith Biochemistry, Vol. 41, Issue 19 https://doi.org/10.1021/bi025585j	journal	May 2002
Protein-Bound Water as the Determinant of Asymmetric Functional Conversion between Light-Driven Proton and Chloride Pumps Muroda, Kosuke; Nakashima, Keisuke; Shibata, Mikihiro Biochemistry, Vol. 51, Issue 23 https://doi.org/10.1021/bi300485r	journal	May 2012
Influence Exercised by Histidine-95 on Chloride Transport and the Photocycle in Halorhodopsin Otomo, Jun Biochemistry, Vol. 35, Issue 21 https://doi.org/10.1021/bi952853n	journal	January 1996
Primary photochemical events in halorhodopsin studied by subpicosecond time-resolved spectroscopy Kandori, Hideki; Yoshihara, Keitaro; Tomioka, Hiroaki The Journal of Physical Chemistry, Vol. 96, Issue 14 https://doi.org/10.1021/j100193a076	journal	July 1992
A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules Cornell, Wendy D.; Cieplak, Piotr; Bayly, Christopher I. Journal of the American Chemical Society, Vol. 117, Issue 19 https://doi.org/10.1021/ja00124a002	journal	May 1995
A new force field for molecular mechanical simulation of nucleic acids and proteins Weiner, Scott J.; Kollman, Peter A.; Case, David A. Journal of the American Chemical Society, Vol. 106, Issue 3 https://doi.org/10.1021/ja00315a051	journal	February 1984
The C ₅ H ₆ NH ₂ ⁺ Protonated Shiff Base: An ab Initio Minimal Model for Retinal Photoisomerization Garavelli, M.; Celani, P.; Bernardi, F. Journal of the American Chemical Society, Vol. 119, Issue 29 https://doi.org/10.1021/ja9610895	journal	July 1997
Electric Field Keeps Chromophore Planar and Produces High Yield Fluorescence in Green Fluorescent Protein Park, Jae Woo; Rhee, Young Min Journal of the American Chemical Society, Vol. 138, Issue 41 https://doi.org/10.1021/jacs.6b06833	journal	October 2016
Ultrafast Protein Dynamics of Bacteriorhodopsin Probed by Photon Echo and Transient Absorption Spectroscopy Kennis, John T. M.; Larsen, Delmar S.; Ohta, Kaoru The Journal of Physical Chemistry B, Vol. 106, Issue 23 https://doi.org/10.1021/jp014681b	journal	June 2002
Protein−β-Ionone Ring Interactions Enhance the Light-Induced Dipole of the Chromophore in Bacteriorhodopsin Aharoni, Amir; Khatchatouriants, Artium; Manevitch, Alexandra The Journal of Physical Chemistry B, Vol. 107, Issue 25 https://doi.org/10.1021/jp027702q	journal	June 2003
Excited-State Charge Transfer at a Conical Intersection: Effects of an Environment Burghardt, Irene; Hynes, James T. The Journal of Physical Chemistry A, Vol. 110, Issue 40 https://doi.org/10.1021/jp057569c	journal	October 2006
Quantification of Sudden Light-Induced Polarization in Bacteriorhodopsin by Optical Rectification Colonna, Anne; Groma, Geza I.; Martin, Jean-Louis The Journal of Physical Chemistry B, Vol. 111, Issue 10 https://doi.org/10.1021/jp0673462	journal	March 2007
Direct QM/MM Excited-State Dynamics of Retinal Protonated Schiff Base in Isolation and Methanol Solution Punwong, Chutintorn; Owens, Jane; Martínez, Todd J. The Journal of Physical Chemistry B, Vol. 119, Issue 3 https://doi.org/10.1021/jp5038798	journal	August 2014
Interfacing the Ab Initio Multiple Spawning Method with Electronic Structure Methods in GAMESS: Photodecay of trans- Azomethane Gaenko, Alexander; DeFusco, Albert; Varganov, Sergey A. The Journal of Physical Chemistry A, Vol. 118, Issue 46 https://doi.org/10.1021/jp508242j	journal	October 2014
Photodynamics in Complex Environments: Ab Initio Multiple Spawning Quantum Mechanical/Molecular Mechanical Dynamics ^† Virshup, Aaron M.; Punwong, Chutintorn; Pogorelov, Taras V. The Journal of Physical Chemistry B, Vol. 113, Issue 11 https://doi.org/10.1021/jp8073464	journal	March 2009
Photoisomerization Quantum Yield and Apparent Energy Content of the K Intermediate in the Photocycles of Bacteriorhodopsin, Its Mutants D85N, R82Q, and D212N, and Deionized Blue Bacteriorhodopsin Logunov, Stephan L.; El-Sayed, Mostafa A.; Song, Li The Journal of Physical Chemistry, Vol. 100, Issue 6 https://doi.org/10.1021/jp9515242	journal	January 1996
Effect of Changing the Position and Orientation of Asp85 Relative to the Protonated Schiff Base within the Retinal Cavity on the Rate of Photoisomerization in Bacteriorhodopsin Song, Li; El-Sayed, M. A.; Lanyi, J. K. The Journal of Physical Chemistry, Vol. 100, Issue 24 https://doi.org/10.1021/jp960734r	journal	January 1996
Adjusted Connection Atoms for Combined Quantum Mechanical and Molecular Mechanical Methods Antes, Iris; Thiel, Walter The Journal of Physical Chemistry A, Vol. 103, Issue 46 https://doi.org/10.1021/jp991771w	journal	November 1999
Ab Initio Multiple Spawning: Photochemistry from First Principles Quantum Molecular Dynamics Ben-Nun, M.; Quenneville, Jason; Martínez, Todd J. The Journal of Physical Chemistry A, Vol. 104, Issue 22 https://doi.org/10.1021/jp994174i	journal	June 2000
Conical intersection dynamics in solution: The chromophore of Green Fluorescent Protein Toniolo, A.; Olsen, S.; Manohar, L. Faraday Discuss., Vol. 127 https://doi.org/10.1039/B401167H	journal	January 2004
Learning from photobiology how to design molecular devices using a computer Gozem, S.; Melaccio, F.; Luk, H. L. Chem. Soc. Rev., Vol. 43, Issue 12 https://doi.org/10.1039/C4CS00037D	journal	January 2014
Monte Carlo study of a phase‐separating liquid mixture by umbrella sampling Torrie, G. M.; Valleau, J. P. The Journal of Chemical Physics, Vol. 66, Issue 4 https://doi.org/10.1063/1.434125	journal	February 1977
Two‐photon double resonance spectroscopy of bacteriorhodopsin. Assignment of the electronic and dipolar properties of the low‐lying ¹ A ^− _g ‐like and ¹ B ^+ _u ‐like π, π* states Birge, Robert R.; Zhang, Chian‐Fan The Journal of Chemical Physics, Vol. 92, Issue 12 https://doi.org/10.1063/1.458206	journal	June 1990
Nonadiabatic molecular dynamics: Validation of the multiple spawning method for a multidimensional problem Ben-Nun, M.; Martı́nez, Todd J. The Journal of Chemical Physics, Vol. 108, Issue 17 https://doi.org/10.1063/1.476142	journal	May 1998
The role of intersection topography in bond selectivity of cis-trans photoisomerization Ben-Nun, M.; Molnar, F.; Schulten, K. Proceedings of the National Academy of Sciences, Vol. 99, Issue 4 https://doi.org/10.1073/pnas.032658099	journal	February 2002
From The Cover: The retinal chromophore/chloride ion pair: Structure of the photoisomerization path and interplay of charge transfer and covalent states Cembran, A.; Bernardi, F.; Olivucci, M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 18 https://doi.org/10.1073/pnas.0408723102	journal	April 2005
Functional electric field changes in photoactivated proteins revealed by ultrafast Stark spectroscopy of the Trp residues Leonard, J.; Portuondo-Campa, E.; Cannizzo, A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 19 https://doi.org/10.1073/pnas.0812877106	journal	April 2009
Aborted double bicycle-pedal isomerization with hydrogen bond breaking is the primary event of bacteriorhodopsin proton pumping Altoe, P.; Cembran, A.; Olivucci, M. Proceedings of the National Academy of Sciences, Vol. 107, Issue 47 https://doi.org/10.1073/pnas.1007000107	journal	November 2010
Retinal has a highly dipolar vertically excited singlet state: implications for vision. Mathies, R.; Stryer, L. Proceedings of the National Academy of Sciences, Vol. 73, Issue 7 https://doi.org/10.1073/pnas.73.7.2169	journal	July 1976
Computational evidence in favor of a two-state, two-mode model of the retinal chromophore photoisomerization Gonzalez-Luque, R.; Garavelli, M.; Bernardi, F. Proceedings of the National Academy of Sciences, Vol. 97, Issue 17 https://doi.org/10.1073/pnas.97.17.9379	journal	August 2000
A Modified Version of the Cornell et al. Force Field with Improved Sugar Pucker Phases and Helical Repeat Cheatham, Thomas E.; Cieplak, Piotr; Kollman, Peter A. Journal of Biomolecular Structure and Dynamics, Vol. 16, Issue 4 https://doi.org/10.1080/07391102.1999.10508297	journal	February 1999
Femtosecond Infrared Spectroscopy of Bacteriorhodopsin Chromophore Isomerization Herbst, J. Science, Vol. 297, Issue 5582 https://doi.org/10.1126/science.1072144	journal	August 2002
Probing the Ultrafast Charge Translocation of Photoexcited Retinal in Bacteriorhodopsin Schenkl, S. Science, Vol. 309, Issue 5736 https://doi.org/10.1126/science.1111482	journal	August 2005
Protein Catalysis of the Retinal Subpicosecond Photoisomerization in the Primary Process of Bacteriorhodopsin Photosynthesis Song, L.; El-Sayed, M. A.; Lanyi, J. K. Science, Vol. 261, Issue 5123 https://doi.org/10.1126/science.261.5123.891	journal	August 1993
Structure of the Light-Driven Chloride Pump Halorhodopsin at 1.8 Å Resolution Kolbe, M. Science, Vol. 288, Issue 5470 https://doi.org/10.1126/science.288.5470.1390	journal	May 2000
Direct observation of the femtosecond excited-state cis-trans isomerization in bacteriorhodopsin Mathies, R.; Brito Cruz, C.; Pollard, W. Science, Vol. 240, Issue 4853 https://doi.org/10.1126/science.3363359	journal	May 1988

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