Unusual Spectroscopic and Electric Field Sensitivity of Chromophores with Short Hydrogen Bonds: GFP and PYP as Model Systems

Lin, Chi-Yun; Boxer, Steven G.

doi:10.1021/acs.jpcb.0c07730

Unusual Spectroscopic and Electric Field Sensitivity of Chromophores with Short Hydrogen Bonds: GFP and PYP as Model Systems

Journal Article · Mon Oct 19 00:00:00 EDT 2020 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.0c07730· OSTI ID:1769614

^[1]; ^[1]

Stanford Univ., CA (United States)

Short hydrogen bonds, with heavy-atom distances less than 2.7 Å, are believed to exhibit proton delocalization, and their possible role in catalysis has been widely debated. While spectroscopic and/or structural methods are usually employed to study the degree of proton delocalization, ambiguities still arise, and no direct information on the corresponding potential energy surface is obtained. Here, we apply an external electric field to perturb the short hydrogen bond(s) within a collection of green fluorescent protein S65T/H148D variants and photoactive yellow protein mutants, where the chromophore participates in the short hydrogen bond(s) and serves as an optical probe of the proton position. As the proton is charged, its position may shift in response to the external electric field, and the chromophore’s electronic absorption can thus reflect the ease of proton transfer. The results suggest that low-barrier hydrogen bonds (LBHBs) are not present within these proteins even when proton affinities between donor and acceptor are closely matched. Exploiting the chromophores as precalibrated electrostatic probes, the covalency of short hydrogen bonds as a nonelectrostatic component is also revealed. A theoretical framework is developed to address a possible contribution of unusually large polarizabilities of short hydrogen bonds due to proton delocalization, but no clear evidence for this phenomenon is found in accordance with the absence of LBHBs.

View Accepted Manuscript (DOE)

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

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

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1769614

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: 43 Vol. 124; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (72)

The Hydrogen Bond in the Solid State Steiner, Thomas Angewandte Chemie International Edition, Vol. 41, Issue 1 https://doi.org/10.1002/1521-3773(20020104)41:1<48::AID-ANIE48>3.0.CO;2-U	journal	January 2002
Electron Transfer and Dynamic Infrared-Band Coalescence: It Looks Like Dynamic NMR Spectroscopy, but a Billion Times Faster Londergan, Casey H.; Kubiak, Clifford P. Chemistry - A European Journal, Vol. 9, Issue 24 https://doi.org/10.1002/chem.200305028	journal	December 2003
Hydrogen Bonding in Biological Structures Jeffrey, George A.; Saenger, Wolfram https://doi.org/10.1007/978-3-642-85135-3	book	January 1991
Localized and delocalized proton levels in hydrogen bonds: Fluorescence line narrowing and stark effect measurements Trommsdorff, H. P. Journal of Luminescence, Vol. 38, Issue 1-6 https://doi.org/10.1016/0022-2313(87)90083-4	journal	December 1987
Stark Spectroscopy on Photoactive Yellow Protein, E46Q, and a Nonisomerizing Derivative, Probes Photo-Induced Charge Motion Premvardhan, L. L.; van der Horst, M. A.; Hellingwerf, K. J. Biophysical Journal, Vol. 84, Issue 5 https://doi.org/10.1016/S0006-3495(03)70047-2	journal	May 2003
Towards an unified hydrogen-bond theory Gilli, G.; Gilli, P. Journal of Molecular Structure, Vol. 552, Issue 1-3 https://doi.org/10.1016/S0022-2860(00)00454-3	journal	September 2000
Understanding enzymic catalysis: the importance of short, strong hydrogen bonds Gerlt, John A.; Kreevoy, Maurice M.; Cleland, W. W. Chemistry & Biology, Vol. 4, Issue 4 https://doi.org/10.1016/S1074-5521(97)90069-7	journal	April 1997
Strong Ionic Hydrogen Bonding Causes a Spectral Isotope Effect in Photoactive Yellow Protein Kaledhonkar, Sandip; Hara, Miwa; Stalcup, T. Page Biophysical Journal, Vol. 105, Issue 11 https://doi.org/10.1016/j.bpj.2013.10.017	journal	December 2013
Hydrogen Bonds: Simple after All? Herschlag, Daniel; Pinney, Margaux M. Biochemistry, Vol. 57, Issue 24 https://doi.org/10.1021/acs.biochem.8b00217	journal	April 2018
Nuclear Quantum Effects in Water and Aqueous Systems: Experiment, Theory, and Current Challenges Ceriotti, Michele; Fang, Wei; Kusalik, Peter G. Chemical Reviews, Vol. 116, Issue 13 https://doi.org/10.1021/acs.chemrev.5b00674	journal	April 2016
Perturbation of Short Hydrogen Bonds in Photoactive Yellow Protein via Noncanonical Amino Acid Incorporation Thomson, Benjamin; Both, Johan; Wu, Yufan The Journal of Physical Chemistry B, Vol. 123, Issue 23 https://doi.org/10.1021/acs.jpcb.9b01571	journal	May 2019
Quantum Effects for a Proton in a Low-Barrier, Double-Well Potential: Core Level Photoemission Spectroscopy of Acetylacetone Feyer, Vitaliy; Prince, Kevin C.; Coreno, Marcello The Journal of Physical Chemistry Letters, Vol. 9, Issue 3 https://doi.org/10.1021/acs.jpclett.7b03175	journal	January 2018
Short Hydrogen Bonds and Proton Delocalization in Green Fluorescent Protein (GFP) Oltrogge, Luke M.; Boxer, Steven G. ACS Central Science, Vol. 1, Issue 3 https://doi.org/10.1021/acscentsci.5b00160	journal	June 2015
Conclusion of the classical-nonclassical ion controversy based on the structural study of the 2-norbornyl cation Olah, George A.; Prakash, G. K. Surya; Saunders, Martin Accounts of Chemical Research, Vol. 16, Issue 12 https://doi.org/10.1021/ar00096a003	journal	December 1983
Are Short, Low-Barrier Hydrogen Bonds Unusually Strong? Perrin, Charles L. Accounts of Chemical Research, Vol. 43, Issue 12 https://doi.org/10.1021/ar100097j	journal	December 2010
Measuring Electric Fields and Noncovalent Interactions Using the Vibrational Stark Effect Fried, Stephen D.; Boxer, Steven G. Accounts of Chemical Research, Vol. 48, Issue 4 https://doi.org/10.1021/ar500464j	journal	March 2015
Stable carbocations, 189. The .sigma.-bridged 2-norbornyl cation and its significance to chemistry Olah, George A. Accounts of Chemical Research, Vol. 9, Issue 2 https://doi.org/10.1021/ar50098a001	journal	February 1976
Predicting Hydrogen-Bond Strengths from Acid−Base Molecular Properties. The p K _a Slide Rule: Toward the Solution of a Long-Lasting Problem Gilli, Paola; Pretto, Loretta; Bertolasi, Valerio Accounts of Chemical Research, Vol. 42, Issue 1 https://doi.org/10.1021/ar800001k	journal	January 2009
Coupling of Hydrogen Bonding to Chromophore Conformation and Function in Photoactive Yellow Protein ^† Brudler, Ronald; Meyer, Terrence E.; Genick, Ulrich K. Biochemistry, Vol. 39, Issue 44 https://doi.org/10.1021/bi0009946	journal	November 2000
Ground-State Proton Transfer Kinetics in Green Fluorescent Protein Oltrogge, Luke M.; Wang, Quan; Boxer, Steven G. Biochemistry, Vol. 53, Issue 37 https://doi.org/10.1021/bi500147n	journal	September 2014
Ultrafast Excited-State Dynamics in the Green Fluorescent Protein Variant S65T/H148D. 1. Mutagenesis and Structural Studies ^† ^, ^‡ Shu, Xiaokun; Kallio, Karen; Shi, Xinghua Biochemistry, Vol. 46, Issue 43 https://doi.org/10.1021/bi7009037	journal	October 2007
Ultrafast Excited-State Dynamics in the Green Fluorescent Protein Variant S65T/H148D. 2. Unusual Photophysical Properties ^† Shi, Xinghua; Abbyad, Paul; Shu, Xiaokun Biochemistry, Vol. 46, Issue 43 https://doi.org/10.1021/bi700904a	journal	October 2007
Photoactive Yellow Protein from the Halophilic Bacterium Salinibacter ruber Memmi, Samy; Kyndt, John; Meyer, Terry Biochemistry, Vol. 47, Issue 7 https://doi.org/10.1021/bi701486n	journal	February 2008
Probing the Ground State Structure of the Green Fluorescent Protein Chromophore Using Raman Spectroscopy ^† Bell, Alasdair F.; He, Xiang; Wachter, Rebekka M. Biochemistry, Vol. 39, Issue 15 https://doi.org/10.1021/bi992675o	journal	April 2000
Modeling the Hydrogen Bond Smith, Douglas A. https://doi.org/10.1021/bk-1994-0569	book	May 1994
Interrelation between H-Bond and Pi-Electron Delocalization Sobczyk, Lucjan; Grabowski, Sławomir Janusz; Krygowski, Tadeusz Marek Chemical Reviews, Vol. 105, Issue 10 https://doi.org/10.1021/cr030083c	journal	October 2005
Update 1 of: Strong Ionic Hydrogen Bonds Meot-Ner (Mautner), Michael Chemical Reviews, Vol. 112, Issue 10 https://doi.org/10.1021/cr200430n	journal	June 2012
Effects of external ions on the energetics of proton transfers across hydrogen bonds Scheiner, Steve; Redfern, Paul; Szczesniak, M. M. The Journal of Physical Chemistry, Vol. 89, Issue 2 https://doi.org/10.1021/j100248a017	journal	January 1985
Evidence for resonance-assisted hydrogen bonding. 4. Covalent nature of the strong homonuclear hydrogen bond. Study of the O-H--O system by crystal structure correlation methods Gilli, Paola; Bertolasi, Valerio; Ferretti, Valeria Journal of the American Chemical Society, Vol. 116, Issue 3 https://doi.org/10.1021/ja00082a011	journal	February 1994
The Chemical Nature of Hydrogen Bonding in Proteins via NMR: J -Couplings, Chemical Shifts, and AIM Theory Arnold, William D.; Oldfield, Eric Journal of the American Chemical Society, Vol. 122, Issue 51 https://doi.org/10.1021/ja0025705	journal	December 2000
Structures and isotopic fractionation factors of complexes AHA-1 Kreevoy, Maurice M.; Liang, Tai-Ming; Chang, Kwang-Chou Journal of the American Chemical Society, Vol. 99, Issue 15 https://doi.org/10.1021/ja00457a065	journal	June 1977
Extremely high polarizability of hydrogen bonds Janoschek, R.; Weidemann, E. G.; Pfeiffer, H. Journal of the American Chemical Society, Vol. 94, Issue 7 https://doi.org/10.1021/ja00762a032	journal	April 1972
Hydrogen-Bond Symmetry in Zwitterionic Phthalate Anions: Symmetry Breaking by Solvation Perrin, Charles L.; Lau, Jonathan S. Journal of the American Chemical Society, Vol. 128, Issue 36 https://doi.org/10.1021/ja063797o	journal	September 2006
Mixed Valency across Hydrogen Bonds Goeltz, John C.; Kubiak, Clifford P. Journal of the American Chemical Society, Vol. 132, Issue 49 https://doi.org/10.1021/ja108841k	journal	December 2010
Are There Really Low-Barrier Hydrogen Bonds in Proteins? The Case of Photoactive Yellow Protein Nadal-Ferret, Marc; Gelabert, Ricard; Moreno, Miquel Journal of the American Chemical Society, Vol. 136, Issue 9 https://doi.org/10.1021/ja4116617	journal	February 2014
Determination of Hydrogen Bond Structure in Water versus Aprotic Environments To Test the Relationship Between Length and Stability Sigala, Paul A.; Ruben, Eliza A.; Liu, Corey W. Journal of the American Chemical Society, Vol. 137, Issue 17 https://doi.org/10.1021/ja512980h	journal	April 2015
Mechanism of Color and Photoacidity Tuning for the Protonated Green Fluorescent Protein Chromophore Lin, Chi-Yun; Boxer, Steven G. Journal of the American Chemical Society, Vol. 142, Issue 25 https://doi.org/10.1021/jacs.0c02796	journal	May 2020
The Low Barrier Hydrogen Bond in the Photoactive Yellow Protein: A Vacuum Artifact Absent in the Crystal and Solution Graen, Timo; Inhester, Ludger; Clemens, Maike Journal of the American Chemical Society, Vol. 138, Issue 51 https://doi.org/10.1021/jacs.6b05609	journal	December 2016
Structural Coupling Throughout the Active Site Hydrogen Bond Networks of Ketosteroid Isomerase and Photoactive Yellow Protein Pinney, Margaux M.; Natarajan, Aditya; Yabukarski, Filip Journal of the American Chemical Society, Vol. 140, Issue 31 https://doi.org/10.1021/jacs.8b01596	journal	July 2018
Stable Mixed-Valent Complexes Formed by Electron Delocalization Across Hydrogen Bonds of Pyrimidinone-Linked Metal Clusters Porter, Tyler M.; Heim, Gavin P.; Kubiak, Clifford P. Journal of the American Chemical Society, Vol. 140, Issue 40 https://doi.org/10.1021/jacs.8b09273	journal	September 2018
Unified Model for Photophysical and Electro-Optical Properties of Green Fluorescent Proteins Lin, Chi-Yun; Romei, Matthew G.; Oltrogge, Luke M. Journal of the American Chemical Society, Vol. 141, Issue 38 https://doi.org/10.1021/jacs.9b07152	journal	August 2019
Isotopic Labeling and Normal-Mode Analysis of a Model Green Fluorescent Protein Chromophore He, Xiang; Bell, Alasdair F.; Tonge, Peter J. The Journal of Physical Chemistry B, Vol. 106, Issue 23 https://doi.org/10.1021/jp0145560	journal	June 2002
Charge Delocalization in the Special-Pair Radical Cation of Mutant Reaction Centers of Rhodobacter s phaeroides from Stark Spectra and Nonadiabatic Spectral Simulations Kanchanawong, Pakorn; Dahlbom, Mats G.; Treynor, Thomas P. The Journal of Physical Chemistry B, Vol. 110, Issue 37 https://doi.org/10.1021/jp0623894	journal	September 2006
Evaluation of the Energetics of the Concerted Acid–Base Mechanism in Enzymatic Catalysis: The Case of Ketosteroid Isomerase Fried, Stephen D.; Boxer, Steven G. The Journal of Physical Chemistry B, Vol. 116, Issue 1 https://doi.org/10.1021/jp210544w	journal	December 2011
Anticipatory active-site motions and chromophore distortion prime photoreceptor PYP for light activation Getzoff, Elizabeth D.; Gutwin, Karl N.; Genick, Ulrich K. Nature Structural & Molecular Biology, Vol. 10, Issue 8 https://doi.org/10.1038/nsb958	journal	July 2003
Low-barrier hydrogen bonds in enzyme cooperativity Dai, Shaobo; Funk, Lisa-Marie; von Pappenheim, Fabian Rabe Nature, Vol. 573, Issue 7775 https://doi.org/10.1038/s41586-019-1581-9	journal	September 2019
Direct evidence of a low barrier hydrogen bond in the catalytic triad of a Serine protease Agback, Peter; Agback, Tatiana Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-28441-7	journal	July 2018
Hydrogen bonding in ionic liquids Hunt, Patricia A.; Ashworth, Claire R.; Matthews, Richard P. Chemical Society Reviews, Vol. 44, Issue 5 https://doi.org/10.1039/C4CS00278D	journal	January 2015
Unraveling the structural and chemical features of biological short hydrogen bonds Zhou, Shengmin; Wang, Lu Chemical Science, Vol. 10, Issue 33 https://doi.org/10.1039/C9SC01496A	journal	January 2019
Theory of Nuclear Magnetic Shielding in Molecules. I. Long‐Range Dipolar Shielding of Protons McConnell, Harden M. The Journal of Chemical Physics, Vol. 27, Issue 1 https://doi.org/10.1063/1.1743676	journal	July 1957
Effect of quantum nuclear motion on hydrogen bonding McKenzie, Ross H.; Bekker, Christiaan; Athokpam, Bijyalaxmi The Journal of Chemical Physics, Vol. 140, Issue 17 https://doi.org/10.1063/1.4873352	journal	May 2014
-Lytic protease can exist in two separately stable conformations with different His57 mobilities and catalytic activities Haddad, K. C.; Sudmeier, J. L.; Bachovchin, D. A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 4 https://doi.org/10.1073/pnas.0409279102	journal	January 2005
Low-barrier hydrogen bond in photoactive yellow protein Yamaguchi, S.; Kamikubo, H.; Kurihara, K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 2 https://doi.org/10.1073/pnas.0811882106	journal	January 2009
Energetics of short hydrogen bonds in photoactive yellow protein Saito, K.; Ishikita, H. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1113599108	journal	December 2011
Thermodynamic framework for identifying free energy inventories of enzyme catalytic cycles Fried, S. D.; Boxer, S. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 30 https://doi.org/10.1073/pnas.1310964110	journal	July 2013
Quantum delocalization of protons in the hydrogen-bond network of an enzyme active site Wang, Lu; Fried, Stephen D.; Boxer, Steven G. Proceedings of the National Academy of Sciences, Vol. 111, Issue 52 https://doi.org/10.1073/pnas.1417923111	journal	December 2014
Energy considerations show that low-barrier hydrogen bonds do not offer a catalytic advantage over ordinary hydrogen bonds Warshel, A.; Papazyan, A. Proceedings of the National Academy of Sciences, Vol. 93, Issue 24 https://doi.org/10.1073/pnas.93.24.13665	journal	November 1996
Low-barrier hydrogen bonds in proteins Hosur, M. V.; Chitra, R.; Hegde, Samarth Crystallography Reviews, Vol. 19, Issue 1 https://doi.org/10.1080/0889311X.2013.771633	journal	January 2013
Proton transfer reactions and hydrogen-bond networks in protein environments Ishikita, Hiroshi; Saito, Keisuke Journal of The Royal Society Interface, Vol. 11, Issue 91 https://doi.org/10.1098/rsif.2013.0518	journal	February 2014
Mixed valence: origins and developments Day, Peter; Hush, Noel S.; Clark, Robin J. H. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 366, Issue 1862 https://doi.org/10.1098/rsta.2007.2135	journal	September 2007
Stark spectroscopy of mixed-valence systems Silverman, Lisa N.; Kanchanawong, Pakorn; Treynor, Thomas P. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 366, Issue 1862 https://doi.org/10.1098/rsta.2007.2137	journal	September 2007
Short hydrogen bonds in photoactive yellow protein Anderson, Spencer; Crosson, Sean; Moffat, Keith Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 6 https://doi.org/10.1107/S090744490400616X	journal	May 2004
Structure of photoactive yellow protein (PYP) E46Q mutant at 1.2 Å resolution suggests how Glu46 controls the spectroscopic and kinetic characteristics of PYP Sugishima, Masakazu; Tanimoto, Norihiko; Soda, Koji Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904024084	journal	November 2004
Do we see what we should see? Describing non-covalent interactions in protein structures including precision Gurusaran, Manickam; Shankar, Mani; Nagarajan, Raju IUCrJ, Vol. 1, Issue 1 https://doi.org/10.1107/S2052252513031485	journal	December 2013
Extreme electric fields power catalysis in the active site of ketosteroid isomerase Fried, Stephen D.; Bagchi, Sayan; Boxer, Steven G. Science, Vol. 346, Issue 6216 https://doi.org/10.1126/science.1259802	journal	December 2014
A Unified Description of Linear and Nonlinear Polarization in Organic Polymethine Dyes Marder, S. R.; Gorman, C. B.; Meyers, F. Science, Vol. 265, Issue 5172 https://doi.org/10.1126/science.265.5172.632	journal	July 1994
Symmetries of Hydrogen Bonds in Solution Perrin, C. L. Science, Vol. 266, Issue 5191 https://doi.org/10.1126/science.266.5191.1665	journal	December 1994
On low-barrier hydrogen bonds and enzyme catalysis Warshel, A.; Papazyan, A.; Kollman, P. Science, Vol. 269, Issue 5220 https://doi.org/10.1126/science.7661987	journal	July 1995
Low-barrier hydrogen bonds and enzymic catalysis Cleland, W.; Kreevoy, M. Science, Vol. 264, Issue 5167 https://doi.org/10.1126/science.8009219	journal	June 1994
STARK SPECTROSCOPY: Applications in Chemistry, Biology, and Materials Science Bublitz, Gerold U.; Boxer, Steven G. Annual Review of Physical Chemistry, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.physchem.48.1.213	journal	October 1997
“Strong” Hydrogen Bonds in Chemistry and Biology Perrin, Charles L.; Nielson, Jennifer B. Annual Review of Physical Chemistry, Vol. 48, Issue 1 https://doi.org/10.1146/annurev.physchem.48.1.511	journal	October 1997
NMR and IR Investigations of Strong Intramolecular Hydrogen Bonds Hansen, Poul Erik; Spanget-Larsen, Jens Molecules, Vol. 22, Issue 4 https://doi.org/10.3390/molecules22040552	journal	March 2017

Similar Records

Short Carboxylic Acid–Carboxylate Hydrogen Bonds Can Have Fully Localized Protons

Journal Article · Sat Dec 17 19:00:00 EST 2016 · Biochemistry · OSTI ID:1339745

Unveiling the mechanism of photoinduced isomerization of the photoactive yellow protein (PYP) chromophore

Journal Article · Sat Dec 13 23:00:00 EST 2014 · Journal of Chemical Physics · OSTI ID:22413300

Neutron and x-ray structural studies of short hydrogen bonds in photoactive yellow protein (PYP).

Journal Article · Thu Nov 01 00:00:00 EDT 2007 · Acta Crystallogr. D · OSTI ID:939324

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Absorption
Chromophores
Imaging probes
Noncovalent interactions
Reaction mechanisms

Unusual Spectroscopic and Electric Field Sensitivity of Chromophores with Short Hydrogen Bonds: GFP and PYP as Model Systems

Citation Formats

References (72)

Similar Records

Related Subjects