Influence of Hydrogen Bonds on the Electron–Phonon Coupling Strength/Marker Mode Structure and Charge Separation Rates in Reaction Centers from Rhodobacter sphaeroides

Khmelnitskiy, Anton; Williams, JoAnn C.; Allen, James P.; Jankowiak, Ryszard

doi:10.1021/acs.jpcb.9b08388

Title: Influence of Hydrogen Bonds on the Electron–Phonon Coupling Strength/Marker Mode Structure and Charge Separation Rates in Reaction Centers from Rhodobacter sphaeroides

Journal Article · Fri Sep 20 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.9b08388· OSTI ID:1801710

Khmelnitskiy, Anton ^[1]; Williams, JoAnn C. ^[2];

^[2];

^[1]

Kansas State University, Manhattan, KS (United States)
Arizona State University, Tempe, AZ (United States)

Low-temperature persistent and transient hole-burning (HB) spectra are presented for the triple hydrogen-bonded L131LH+M160LH+M197FH mutant of Rhodobacter sphaeroides. These spectra expose the heterogeneous nature of the P-, B-, and H-bands, consistent with a distribution of electron transfer (ET) times and excitation energy transfer (EET) rates. Transient P⁺QA^– holes are observed for fast (tens of ps or faster) ET times and reveal strong coupling to phonons and marker mode(s), while the persistent holes are bleached in a fraction of reaction centers (RCs) with long-lived excited states characterized by much weaker electron-phonon coupling. We report exposed differences in electron-phonon coupling strength, as well as a different coupling to the marker mode(s) appear to affect the ET times. Both resonantly and nonresonantly burned persistent HB spectra show weak blue- (~150 cm^-1) and large, red-shifted (~300 cm^-1) anti-holes of the P band. Slower EET times from the H- and B-bands to the special pair dimer provide new insight on the influence of hydrogen bonds on mutation-induced heterogeneity.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Kansas State Univ., Manhattan, KS (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)

Grant/Contract Number:: SC0006678; CHE-1904860

OSTI ID:: 1801710

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Vol. 123, Issue 41; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (50)

Coherent Dynamics during the Primary Electron-Transfer Reaction in Membrane-Bound Reaction Centers of Rhodobacter sphaeroides Vos, Marten H.; Jones, Michael R.; Hunter, C. Neil Biochemistry, Vol. 33, Issue 22 https://doi.org/10.1021/bi00188a002	journal	June 1994
Mechanism of Charge Separation and Stabilization of Separated Charges in Reaction Centers of Chloroflexus a urantiacus and of YM210W(L) Mutants of Rhodobacter s phaeroides Excited by 20 fs Pulses at 90 K ^† Yakovlev, A. G.; Vasilieva, L. G.; Shkuropatov, A. Ya. The Journal of Physical Chemistry A, Vol. 107, Issue 40 https://doi.org/10.1021/jp0300647	journal	October 2003
Conformation of Bacteriochlorophyll Molecules in Photosynthetic Proteins from Purple Bacteria ^† Lapouge, Karine; Näveke, Arne; Gall, Andrew Biochemistry, Vol. 38, Issue 34 https://doi.org/10.1021/bi990723z	journal	August 1999
Spectral hole-burning spectroscopy in amorphous molecular solids and proteins Jankowiak, R.; Hayes, J. M.; Small, G. J. Chemical Reviews, Vol. 93, Issue 4 https://doi.org/10.1021/cr00020a005	journal	June 1993
Photochemical hole-burned spectra of protonated and deuterated reaction centers of Rhodobacter sphaeroides Lyle, P. A.; Kolaczkowski, S. V.; Small, G. J. The Journal of Physical Chemistry, Vol. 97, Issue 26 https://doi.org/10.1021/j100128a030	journal	July 1993
Direct observation of vibrational coherence in bacterial reaction centers using femtosecond absorption spectroscopy. Vos, M. H.; Lambry, J. C.; Robles, S. J. Proceedings of the National Academy of Sciences, Vol. 88, Issue 20 https://doi.org/10.1073/pnas.88.20.8885	journal	October 1991
Band Structure of the Rhodobacter sphaeroides Photosynthetic Reaction Center from Low-Temperature Absorption and Hole-Burned Spectra Rancova, Olga; Jankowiak, Ryszard; Kell, Adam The Journal of Physical Chemistry B, Vol. 120, Issue 25 https://doi.org/10.1021/acs.jpcb.6b02595	journal	June 2016
Applications of spectral hole burning spectroscopies to antenna and reaction center complexes Reddy, N. Raja S.; Lyle, Paul A.; Small, Gerald J. Photosynthesis Research, Vol. 31, Issue 3 https://doi.org/10.1007/BF00035536	journal	March 1992
Spectroscopic Study of the CP43′ Complex and the PSI–CP43′ Supercomplex of the Cyanobacterium Synechocystis PCC 6803 Feng, Ximao; Neupane, Bhanu; Acharya, Khem The Journal of Physical Chemistry B, Vol. 115, Issue 45 https://doi.org/10.1021/jp206054b	journal	November 2011
The role of reaction center excited state evolution during charge separation in a Rb. sphaeroides mutant with an initial electron donor midpoint potential 260 mV above wild type Woodbury, Neal W.; Lin, Su; Lin, Xiaomei Chemical Physics, Vol. 197, Issue 3 https://doi.org/10.1016/0301-0104(95)00170-S	journal	August 1995
Pathway of proton transfer in bacterial reaction centers: replacement of glutamic acid 212 in the L subunit by glutamine inhibits quinone (secondary acceptor) turnover Paddock, M. L.; Rongey, S. H.; Feher, G. Proceedings of the National Academy of Sciences, Vol. 86, Issue 17 https://doi.org/10.1073/pnas.86.17.6602	journal	September 1989
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
Coupling of nuclear wavepacket motion and charge separation in bacterial reaction centers Shuvalov, V. A.; Yakovlev, A. G. FEBS Letters, Vol. 540, Issue 1-3 https://doi.org/10.1016/S0014-5793(03)00237-0	journal	March 2003
Correlation between Multiple Hydrogen Bonding and Alteration of the Oxidation Potential of the Bacteriochlorophyll Dimer of Reaction Centers from Rhodobacter sphaeroides Mattioli, T. A.; Lin, X.; Allen, J. P. Biochemistry, Vol. 34, Issue 18 https://doi.org/10.1021/bi00018a017	journal	May 1995
Direct observation of tiers in the energy landscape of a chromoprotein: A single-molecule study Hofmann, C.; Aartsma, T. J.; Michel, H. Proceedings of the National Academy of Sciences, Vol. 100, Issue 26 https://doi.org/10.1073/pnas.2533896100	journal	December 2003
Electronic Interactions in the Bacterial Reaction Center Revealed by Two-Color 2D Electronic Spectroscopy Konar, Arkaprabha; Sechrist, Riley; Song, Yin The Journal of Physical Chemistry Letters, Vol. 9, Issue 18 https://doi.org/10.1021/acs.jpclett.8b02394	journal	August 2018
Structural details of an interaction between cardiolipin and an integral membrane protein McAuley, K. E.; Fyfe, P. K.; Ridge, J. P. Proceedings of the National Academy of Sciences, Vol. 96, Issue 26 https://doi.org/10.1073/pnas.96.26.14706	journal	December 1999
Site Selective and Single Complex Laser-Based Spectroscopies: A Window on Excited State Electronic Structure, Excitation Energy Transfer, and Electron–Phonon Coupling of Selected Photosynthetic Complexes Jankowiak, Ryszard; Reppert, Mike; Zazubovich, Valter Chemical Reviews, Vol. 111, Issue 8 https://doi.org/10.1021/cr100234j	journal	August 2011
The question of dispersive kinetics for the initial phase of charge separation in bacterial reaction centers Small, G. J.; Hayes, J. M.; Silbey, R. J. The Journal of Physical Chemistry, Vol. 96, Issue 19 https://doi.org/10.1021/j100198a005	journal	September 1992
Molecular Mechanisms of Photosynthesis Blankenship, Robert E. https://doi.org/10.1002/9780470758472	book	December 2002
Intervalence Band Stark Effect of the Special Pair Radical Cation in Bacterial Photosynthetic Reaction Centers Treynor, Thomas P.; Andrews, Steven S.; Boxer, Steven G. The Journal of Physical Chemistry B, Vol. 107, Issue 40 https://doi.org/10.1021/jp035039f	journal	October 2003
Radicals, Radical Pairs and Triplet States in Photosynthesis Lubitz, Wolfgang; Lendzian, Friedhelm; Bittl, Robert Accounts of Chemical Research, Vol. 35, Issue 5 https://doi.org/10.1021/ar000084g	journal	May 2002
Tuning of the optical and electrochemical properties of the primary donor bacteriochlorophylls in the reaction centre from Rhodobacter sphaeroides: spectroscopy and structure Spiedel, Diane; Roszak, Aleksander W.; McKendrick, Kimberley Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1554, Issue 1-2 https://doi.org/10.1016/S0005-2728(02)00215-3	journal	April 2002
Electron Transfer Between Biological Molecules by Thermally Activated Tunneling Hopfield, J. J. Proceedings of the National Academy of Sciences, Vol. 71, Issue 9 https://doi.org/10.1073/pnas.71.9.3640	journal	September 1974
Structure of the reaction center from Rhodobacter sphaeroides R-26 and 2.4.1: protein-cofactor (bacteriochlorophyll, bacteriopheophytin, and carotenoid) interactions. Yeates, T. O.; Komiya, H.; Chirino, A. Proceedings of the National Academy of Sciences, Vol. 85, Issue 21 https://doi.org/10.1073/pnas.85.21.7993	journal	November 1988
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
Effects of mutations near the bacteriochlorophylls in reaction centers from Rhodobacter sphaeroides Williams, J. C.; Alden, R. G.; Murchison, H. A. Biochemistry, Vol. 31, Issue 45 https://doi.org/10.1021/bi00160a012	journal	November 1992
Nuclear wavepacket motion producing a reversible charge separation in bacterial reaction centers Yakovlev, A. G.; Shkuropatov, A. Y.; Shuvalov, V. A. FEBS Letters, Vol. 466, Issue 2-3 https://doi.org/10.1016/S0014-5793(00)01081-4	journal	January 2000
Charge separation in Rhodobacter sphaeroides mutant reaction centers with increased midpoint potential of the primary electron donor Khmelnitskiy, A. Yu.; Khatypov, R. A.; Khristin, A. M. Biochemistry (Moscow), Vol. 78, Issue 1 https://doi.org/10.1134/S0006297913010070	journal	January 2013
Specific alteration of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. Lin, X.; Murchison, H. A.; Nagarajan, V. Proceedings of the National Academy of Sciences, Vol. 91, Issue 22 https://doi.org/10.1073/pnas.91.22.10265	journal	October 1994
Challenges facing an understanding of the nature of low-energy excited states in photosynthesis Reimers, Jeffrey R.; Biczysko, Malgorzata; Bruce, Douglas Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 9 https://doi.org/10.1016/j.bbabio.2016.06.010	journal	September 2016
Coherent phenomena of charge separation in reaction centers of LL131H and LL131H/LM160H/FM197H mutants of Rhodobacter sphaeroides Yakovlev, A. G.; Vasilieva, L. G.; Shkuropatov, A. Y. Biochemistry (Moscow), Vol. 76, Issue 10 https://doi.org/10.1134/S000629791110004X	journal	October 2011
Electronic energy transfer through non-adiabatic vibrational-electronic resonance. I. Theory for a dimer Tiwari, Vivek; Peters, William K.; Jonas, David M. The Journal of Chemical Physics, Vol. 147, Issue 15 https://doi.org/10.1063/1.5005835	journal	October 2017
pH Modulates the Quinone Position in the Photosynthetic Reaction Center from Rhodobacter sphaeroides in the Neutral and Charge Separated States Koepke, Juergen; Krammer, Eva-Maria; Klingen, Astrid R. Journal of Molecular Biology, Vol. 371, Issue 2 https://doi.org/10.1016/j.jmb.2007.04.082	journal	August 2007
Mechanism and Reaction Coordinate of Directional Charge Separation in Bacterial Reaction Centers Eisenmayer, Thomas J.; de Groot, Huub J. M.; van de Wetering, Elbert The Journal of Physical Chemistry Letters, Vol. 3, Issue 6 https://doi.org/10.1021/jz201695p	journal	February 2012
Picosecond kinetics of the initial photochemical electron-transfer reaction in bacterial photosynthetic reaction centers Woodbury, N. W.; Becker, M.; Middendorf, D. Biochemistry, Vol. 24, Issue 26 https://doi.org/10.1021/bi00347a002	journal	December 1985
Vibronic Coherence in the Charge Separation Process of the Rhodobacter sphaeroides Reaction Center Ma, Fei; Romero, Elisabet; Jones, Michael R. The Journal of Physical Chemistry Letters, Vol. 9, Issue 8 https://doi.org/10.1021/acs.jpclett.8b00108	journal	March 2018
Crystallographic Analyses of Site-Directed Mutants of the Photosynthetic Reaction Center from Rhodobacter sphaeroides Chirino, Arthur J.; Lous, Erik J.; Huber, Martina Biochemistry, Vol. 33, Issue 15 https://doi.org/10.1021/bi00181a020	journal	April 1994
A Unified Description of the Electrochemical, Charge Distribution, and Spectroscopic Properties of the Special-Pair Radical Cation in Bacterial Photosynthesis Reimers, Jeffrey R.; Hush, Noel S. Journal of the American Chemical Society, Vol. 126, Issue 13 https://doi.org/10.1021/ja036883m	journal	April 2004
Visualization of coherent nuclear motion in a membrane protein by femtosecond spectroscopy Vos, Marten H.; Rappaport, Fabrice; Lambry, Jean-Christophe Nature, Vol. 363, Issue 6427 https://doi.org/10.1038/363320a0	journal	May 1993
Mutations designed to modify the environment of the primary electron donor of the reaction center from Rhodobacter sphaeroides: Phenylalanine to leucine at L167 and histidine to phenylalanine at L168 Murchison, H. A.; Alden, R. G.; Allen, J. P. Biochemistry, Vol. 32, Issue 13 https://doi.org/10.1021/bi00064a038	journal	April 1993
ENDOR Studies of the Primary Donor Cation Radical in Mutant Reaction Centers of Rhodobacter sphaeroides with Altered Hydrogen-Bond Interactions Rautter, J.; Lendzian, F.; Schulz, C. Biochemistry, Vol. 34, Issue 25 https://doi.org/10.1021/bi00025a020	journal	January 1995
The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment–protein complexes Chin, A. W.; Prior, J.; Rosenbach, R. Nature Physics, Vol. 9, Issue 2 https://doi.org/10.1038/nphys2515	journal	January 2013
Excitation Wavelength Dependence of Energy Transfer and Charge Separation in Reaction Centers from Rhodobacter sphaeroides : Evidence for Adiabatic Electron Transfer Lin, Su; Taguchi, Aileen K. W.; Woodbury, Neal W. The Journal of Physical Chemistry, Vol. 100, Issue 42 https://doi.org/10.1021/jp961590j	journal	January 1996
Electronic Energy Transfer within the Hexamer Cofactor System of Bacterial Reaction Centers Vos, Marten H.; Breton, Jacques; Martin, Jean-Louis The Journal of Physical Chemistry B, Vol. 101, Issue 47 https://doi.org/10.1021/jp971486h	journal	November 1997
Design of a Redox-Linked Active Metal Site: Manganese Bound to Bacterial Reaction Centers at a Site Resembling That of Photosystem II ^† ^, ^‡ Thielges, M.; Uyeda, G.; Cámara-Artigas, A. Biochemistry, Vol. 44, Issue 20 https://doi.org/10.1021/bi050377n	journal	May 2005
Protein Dynamics Control the Kinetics of Initial Electron Transfer in Photosynthesis Wang, H.; Lin, S.; Allen, J. P. Science, Vol. 316, Issue 5825 https://doi.org/10.1126/science.1140030	journal	May 2007
Both electronic and vibrational coherences are involved in primary electron transfer in bacterial reaction center Ma, Fei; Romero, Elisabet; Jones, Michael R. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-08751-8	journal	February 2019
Temperature Dependence of the Reorganization Energy for Charge Recombination in the Reaction Center from Rhodobacter sphaeroides ^† Ortega, J. M.; Mathis, P.; Williams, J. C. Biochemistry, Vol. 35, Issue 11 https://doi.org/10.1021/bi952882y	journal	January 1996
Role of Protein Dynamics in Guiding Electron-Transfer Pathways in Reaction Centers from Rhodobacter sphaeroides Wang, Haiyu; Hao, Yawei; Jiang, Ying, The Journal of Physical Chemistry B, Vol. 116, Issue 1 https://doi.org/10.1021/jp211702b	journal	December 2011

Similar Records

Photochemical hole-burned spectra of protonated and deuterated reaction centers of Rhodobacter sphaeroides

Journal Article · Thu Jul 01 00:00:00 EDT 1993 · Journal of Physical Chemistry; (United States) · OSTI ID:1801710

Lyle, P A; Kolaczkowski, S V; Small, G J

B-side electron transfer promoted by absorbance of multiple photons in Rhodobacter sphaeroides R-26 reaction centers

Journal Article · Thu Jun 03 00:00:00 EDT 1999 · Journal of Physical Chemistry B: Materials, Surfaces, Interfaces, amp Biophysical · OSTI ID:1801710

Lin, S; Jackson, J A; Taguchi, A K.W.; +1 more

Excited state structure, energy and electron transfer dynamics of photosynthetic reaction centers: A hole burning study

Technical Report · Fri Mar 22 00:00:00 EST 1991 · OSTI ID:1801710

Tang, De-Ming

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
absorption
fluorescence resonance energy transfer
peptides
proteins
quantum mechanics
redox reactions

Title: Influence of Hydrogen Bonds on the Electron–Phonon Coupling Strength/Marker Mode Structure and Charge Separation Rates in Reaction Centers from Rhodobacter sphaeroides

Citation Formats

References (50)

Similar Records

Related Subjects