Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Probing microhydration effect on the electronic structure of the GFP chromophore anion. Photoelectron spectroscopy and theoretical investigations

Abstract

The photophysics of Green Fluorescent Protein (GFP) chromophore is critically dependent on its local structure and on its environment. Despite extensive experimental and computational studies, there remain many open questions regarding the key fundamental variables that govern this process. One outstanding problem is the role of autoionization as a possible relaxation pathway of the excited state under different environmental conditions. This issue is considered in our work through combined experimental and theoretical studies of microsolvated clusters of the deprotonated p-hydroxybenzylidene-2,3-dimethylimidazolinone anion (HBDI⁻), an analog of GFP chromophore. Through selective generation of microsolvated structures of predetermined size and subsequent analysis of experimental photoelectron spectra by high level ab-initio methods we are able to precisely identify the structure of the system, establish the accuracy of theoretical data, and provide reliable description of auto-ionization process as a function of hydrogen-bonding environment. Our study clearly illustrates the first few water molecules progressively stabilize the excited state of the chromophore anion against the autodetached neutral state, which should be an important trait for crystallographic water molecules in GFPs that has not been fully explored to date.

Authors:
 [1];  [2];  [3];  [1];  [2];  [3]
+ Show Author Affiliations
  1. Louisiana State Univ., Baton Rouge, LA (United States)
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Atmospheric Science and Global Change Div. (ASGC)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1229926
Alternate Identifier(s):
OSTI ID: 1228439
Report Number(s):
PNNL-SA-113513
Journal ID: ISSN 0021-9606; 48585; KC0301050; KC0301050
Grant/Contract Number:  
AC05-76RL01830; AC06.76RLO-1830; SC0012432
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Chemical Physics
Additional Journal Information:
Journal Volume: 143; Journal Issue: 22; Journal ID: ISSN 0021-9606
Publisher:
American Institute of Physics (AIP)
Country of Publication:
United States
Language:
English
Subject:
Environmental Molecular Sciences Laboratory

Citation Formats

Bhaskaran-Nair, Kiran, Valiev, Marat, Deng, Shihu, Shelton, William A., Kowalski, Karol, and Wang, Xue B. Probing microhydration effect on the electronic structure of the GFP chromophore anion. Photoelectron spectroscopy and theoretical investigations. United States: N. p., 2015. Web. doi:10.1063/1.4936252.
Copy to clipboard
Bhaskaran-Nair, Kiran, Valiev, Marat, Deng, Shihu, Shelton, William A., Kowalski, Karol, & Wang, Xue B. Probing microhydration effect on the electronic structure of the GFP chromophore anion. Photoelectron spectroscopy and theoretical investigations. United States. https://doi.org/10.1063/1.4936252
Copy to clipboard
Bhaskaran-Nair, Kiran, Valiev, Marat, Deng, Shihu, Shelton, William A., Kowalski, Karol, and Wang, Xue B. Mon . "Probing microhydration effect on the electronic structure of the GFP chromophore anion. Photoelectron spectroscopy and theoretical investigations". United States. https://doi.org/10.1063/1.4936252. https://www.osti.gov/servlets/purl/1229926.
Copy to clipboard
@article{osti_1229926,
title = {Probing microhydration effect on the electronic structure of the GFP chromophore anion. Photoelectron spectroscopy and theoretical investigations},
author = {Bhaskaran-Nair, Kiran and Valiev, Marat and Deng, Shihu and Shelton, William A. and Kowalski, Karol and Wang, Xue B.},
abstractNote = {The photophysics of Green Fluorescent Protein (GFP) chromophore is critically dependent on its local structure and on its environment. Despite extensive experimental and computational studies, there remain many open questions regarding the key fundamental variables that govern this process. One outstanding problem is the role of autoionization as a possible relaxation pathway of the excited state under different environmental conditions. This issue is considered in our work through combined experimental and theoretical studies of microsolvated clusters of the deprotonated p-hydroxybenzylidene-2,3-dimethylimidazolinone anion (HBDI⁻), an analog of GFP chromophore. Through selective generation of microsolvated structures of predetermined size and subsequent analysis of experimental photoelectron spectra by high level ab-initio methods we are able to precisely identify the structure of the system, establish the accuracy of theoretical data, and provide reliable description of auto-ionization process as a function of hydrogen-bonding environment. Our study clearly illustrates the first few water molecules progressively stabilize the excited state of the chromophore anion against the autodetached neutral state, which should be an important trait for crystallographic water molecules in GFPs that has not been fully explored to date.},
doi = {10.1063/1.4936252},
journal = {Journal of Chemical Physics},
number = 22,
volume = 143,
place = {United States},
year = {Mon Dec 14 00:00:00 EST 2015},
month = {Mon Dec 14 00:00:00 EST 2015}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1063/1.4936252
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 16 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

New coupled-cluster methods with singles, doubles, and noniterative triples for high accuracy calculations of excited electronic states
journal, January 2004

  • Kowalski, Karol; Piecuch, Piotr
  • The Journal of Chemical Physics, Vol. 120, Issue 4
  • DOI: 10.1063/1.1632474

Internal Conversion in the Chromophore of the Green Fluorescent Protein:  Temperature Dependence and Isoviscosity Analysis
journal, April 2003

  • Litvinenko, Konstantin L.; Webber, Naomi M.; Meech, Stephen R.
  • The Journal of Physical Chemistry A, Vol. 107, Issue 15
  • DOI: 10.1021/jp027376e

Wavelength mutations and posttranslational autoxidation of green fluorescent protein.
journal, December 1994

  • Heim, R.; Prasher, D. C.; Tsien, R. Y.
  • Proceedings of the National Academy of Sciences, Vol. 91, Issue 26
  • DOI: 10.1073/pnas.91.26.12501

Cis − Trans Photoisomerization of Fluorescent-Protein Chromophores
journal, August 2008

  • Voliani, Valerio; Bizzarri, Ranieri; Nifosì, Riccardo
  • The Journal of Physical Chemistry B, Vol. 112, Issue 34
  • DOI: 10.1021/jp802419h

Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein
journal, November 2004

  • Shaner, Nathan C.; Campbell, Robert E.; Steinbach, Paul A.
  • Nature Biotechnology, Vol. 22, Issue 12
  • DOI: 10.1038/nbt1037

On the optical absorption of the anionic GFP chromophore in vacuum, solution, and protein
journal, January 2013

  • Petrone, Alessio; Caruso, Pasquale; Tenuta, Silvia
  • Physical Chemistry Chemical Physics, Vol. 15, Issue 47
  • DOI: 10.1039/c3cp52820k

The Green Fluorescent Protein
journal, June 1998

Diffraction-unlimited all-optical imaging and writing with a photochromic GFP
journal, September 2011

  • Grotjohann, Tim; Testa, Ilaria; Leutenegger, Marcel
  • Nature, Vol. 478, Issue 7368
  • DOI: 10.1038/nature10497

Electronic Excitations of the Chromophore from the Fluorescent Protein asFP595 in Solutions
journal, December 2005

  • Nemukhin, Alexander V.; Topol, Igor A.; Burt, Stanley K.
  • Journal of Chemical Theory and Computation, Vol. 2, Issue 2
  • DOI: 10.1021/ct050243n

Origin, Nature, and Fate of the Fluorescent State of the Green Fluorescent Protein Chromophore at the CASPT2//CASSCF Resolution
journal, May 2004

  • Martin, María Elena; Negri, Fabrizia; Olivucci, Massimo
  • Journal of the American Chemical Society, Vol. 126, Issue 17
  • DOI: 10.1021/ja037278m

Photoabsorption studies of neutral green fluorescent protein model chromophores in vacuo
journal, January 2009

  • Rajput, J.; Rahbek, D. B.; Andersen, L. H.
  • Physical Chemistry Chemical Physics, Vol. 11, Issue 43
  • DOI: 10.1039/b914276b

Absorption of the green fluorescent protein chromophore anion in the gas phase studied by a combination of FTICR mass spectrometry with laser-induced photodissociation spectroscopy
journal, September 2011

  • Chingin, Konstantin; Balabin, Roman M.; Frankevich, Vladimir
  • International Journal of Mass Spectrometry, Vol. 306, Issue 2-3
  • DOI: 10.1016/j.ijms.2011.01.014

Quantum chemical modeling of structure and absorption spectra of the chromophore in green fluorescent proteins
journal, May 1998

Photoactivatable fluorescent proteins
journal, September 2005

  • Lukyanov, Konstantin A.; Chudakov, Dmitry M.; Lukyanov, Sergey
  • Nature Reviews Molecular Cell Biology, Vol. 6, Issue 11
  • DOI: 10.1038/nrm1741

Development of a low-temperature photoelectron spectroscopy instrument using an electrospray ion source and a cryogenically controlled ion trap
journal, July 2008

  • Wang, Xue-Bin; Wang, Lai-Sheng
  • Review of Scientific Instruments, Vol. 79, Issue 7
  • DOI: 10.1063/1.2957610

Equation of motion coupled cluster methods for electron attachment and ionization potential in fullerenes C 60 and C 70
journal, August 2014

  • Bhaskaran-Nair, Kiran; Kowalski, Karol; Moreno, Juana
  • The Journal of Chemical Physics, Vol. 141, Issue 7
  • DOI: 10.1063/1.4891934

Viscosity-Dependent Fluorescence Decay of the GFP Chromophore in Solution Due to Fast Internal Conversion
journal, August 2002

  • Kummer, Andreas D.; Kompa, Christian; Niwa, Haruki
  • The Journal of Physical Chemistry B, Vol. 106, Issue 30
  • DOI: 10.1021/jp014713v

A fifth-order perturbation comparison of electron correlation theories
journal, May 1989

Efficient formulation and computer implementation of the active-space electron-attached and ionized equation-of-motion coupled-cluster methods
journal, December 2006

  • Gour, Jeffrey R.; Piecuch, Piotr
  • The Journal of Chemical Physics, Vol. 125, Issue 23
  • DOI: 10.1063/1.2409289

Data storage based on photochromic and photoconvertible fluorescent proteins
journal, September 2010

Electronic excitations of green fluorescent proteins: Protonation states of chromophore model compound in solutions
journal, November 2005

  • Xie, Daiqian; Zeng, Jun
  • Journal of Computational Chemistry, Vol. 26, Issue 14
  • DOI: 10.1002/jcc.20273

Direct and Indirect Electron Emission from the Green Fluorescent Protein Chromophore
journal, September 2012

NWChem: A comprehensive and scalable open-source solution for large scale molecular simulations
journal, September 2010

  • Valiev, M.; Bylaska, E. J.; Govind, N.
  • Computer Physics Communications, Vol. 181, Issue 9, p. 1477-1489
  • DOI: 10.1016/j.cpc.2010.04.018

Excited-State Dynamics in the Green Fluorescent Protein Chromophore
journal, January 2004

  • Mandal, Debabrata; Tahara, Tahei; Meech, Stephen R.
  • The Journal of Physical Chemistry B, Vol. 108, Issue 3
  • DOI: 10.1021/jp035816b

Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins
journal, November 2005

  • Hofmann, M.; Eggeling, C.; Jakobs, S.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 49
  • DOI: 10.1073/pnas.0506010102

The Gas-Phase Absorption Spectrum of a Neutral GFP Model Chromophore
journal, January 2007

Extraction, Purification and Properties of Aequorin, a Bioluminescent Protein from the Luminous Hydromedusan,Aequorea
journal, June 1962

  • Shimomura, Osamu; Johnson, Frank H.; Saiga, Yo
  • Journal of Cellular and Comparative Physiology, Vol. 59, Issue 3
  • DOI: 10.1002/jcp.1030590302

Photoelectron spectroscopy of the model GFP chromophore anion
journal, January 2012

  • Horke, Daniel A.; Verlet, Jan R. R.
  • Physical Chemistry Chemical Physics, Vol. 14, Issue 24
  • DOI: 10.1039/c2cp40880e

Structural basis for dual excitation and photoisomerization of the Aequorea victoria green fluorescent protein
journal, March 1997

  • Brejc, K.; Sixma, T. K.; Kitts, P. A.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 6
  • DOI: 10.1073/pnas.94.6.2306

Taking the green fluorescence out of the protein: dynamics of the isolated GFP chromophore anion
journal, January 2013

  • Mooney, Ciarán R. S.; Horke, Daniel A.; Chatterley, Adam S.
  • Chem. Sci., Vol. 4, Issue 3
  • DOI: 10.1039/C2SC21737F

The structure and function of fluorescent proteins
journal, January 2009

  • Sample, Vedangi; Newman, Robert H.; Zhang, Jin
  • Chemical Society Reviews, Vol. 38, Issue 10
  • DOI: 10.1039/b913033k

Fluorescent properties of model chromophores of tyrosine-66 substituted mutants of Aequorea green fluorescent protein (GEP)
journal, July 1998

Chemical nature of the light emitter of the Aequorea green fluorescent protein
journal, November 1996

  • Niwa, H.; Inouye, S.; Hirano, T.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 24
  • DOI: 10.1073/pnas.93.24.13617

Ultrafast dual photoresponse of isolated biological chromophores: link to the photoinduced mode-specific non-adiabatic dynamics in proteins
journal, January 2013

  • Bochenkova, Anastasia V.; Andersen, Lars H.
  • Faraday Discussions, Vol. 163
  • DOI: 10.1039/c3fd20150c

Photodetachment Spectra of Deprotonated Fluorescent Protein Chromophore Anions
journal, July 2012

  • Mooney, Ciarán R. S.; Sanz, M. Eugenia; McKay, Adam R.
  • The Journal of Physical Chemistry A, Vol. 116, Issue 30
  • DOI: 10.1021/jp3058349

Equation-of-motion coupled cluster method with full inclusion of the connected triple excitations for ionized states: IP-EOM-CCSDT
journal, January 2003

  • Musiał, Monika; Kucharski, Stanisław A.; Bartlett, Rodney J.
  • The Journal of Chemical Physics, Vol. 118, Issue 3
  • DOI: 10.1063/1.1527013

UV Excited-State Photoresponse of Biochromophore Negative Ions
journal, July 2014

  • Bochenkova, Anastasia V.; Klaerke, Benedikte; Rahbek, Dennis B.
  • Angewandte Chemie International Edition, Vol. 53, Issue 37
  • DOI: 10.1002/anie.201404609

Evolution of new nonantibody proteins via iterative somatic hypermutation
journal, November 2004

  • Wang, L.; Jackson, W. C.; Steinbach, P. A.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 48, p. 16745-16749
  • DOI: 10.1073/pnas.0407752101

Solvatochromism of the Green Fluorescence Protein Chromophore and Its Derivatives
journal, September 2006

  • Dong, Jian; Solntsev, Kyril M.; Tolbert, Laren M.
  • Journal of the American Chemical Society, Vol. 128, Issue 37
  • DOI: 10.1021/ja063128a

Crystal Structure of the Aequorea victoria Green Fluorescent Protein
journal, September 1996

Constructing and Exploiting the Fluorescent Protein Paintbox (Nobel Lecture)
journal, July 2009

Potential Energy Landscape of the Electronic States of the GFP Chromophore in Different Protonation Forms: Electronic Transition Energies and Conical Intersections
journal, July 2010

  • Polyakov, I. V.; Grigorenko, B. L.; Epifanovsky, E. M.
  • Journal of Chemical Theory and Computation, Vol. 6, Issue 8
  • DOI: 10.1021/ct100227k

Green Fluorescent Protein (GFP):  Applications, Structure, and Related Photophysical Behavior
journal, March 2002

Green fluorescent protein as a marker for gene expression
journal, February 1994

Ultra-fast excited state dynamics in green fluorescent protein: multiple states and proton transfer.
journal, August 1996

  • Chattoraj, M.; King, B. A.; Bublitz, G. U.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 16
  • DOI: 10.1073/pnas.93.16.8362

Resonantly Enhanced Multiphoton Ionization Spectrum of the Neutral Green Fluorescent Protein Chromophore
journal, September 2014

  • Greenwood, Jason B.; Miles, Jordan; Camillis, Simone De
  • The Journal of Physical Chemistry Letters, Vol. 5, Issue 20
  • DOI: 10.1021/jz5019256

Excited State Dynamics of the Isolated Green Fluorescent Protein Chromophore Anion Following UV Excitation
journal, February 2015

  • West, Christopher W.; Bull, James N.; Hudson, Alex S.
  • The Journal of Physical Chemistry B, Vol. 119, Issue 10
  • DOI: 10.1021/acs.jpcb.5b01432

Perturbative treatment of the similarity transformed Hamiltonian in equation‐of‐motion coupled‐cluster approximations
journal, July 1995

  • Stanton, John F.; Gauss, Jürgen
  • The Journal of Chemical Physics, Vol. 103, Issue 3
  • DOI: 10.1063/1.469817

Efficient Diffuse Basis Sets: cc-pV x Z+ and maug-cc-pV x Z
journal, March 2009

  • Papajak, Ewa; Leverentz, Hannah R.; Zheng, Jingjing
  • Journal of Chemical Theory and Computation, Vol. 5, Issue 5
  • DOI: 10.1021/ct800575z

The equation-of-motion coupled-cluster method: Excitation energies of Be and CO
journal, December 1989

Potential energy curves via double electron-attachment calculations: Dissociation of alkali metal dimers
journal, May 2013

  • Musiał, Monika; Kowalska-Szojda, Katarzyna; Lyakh, Dmitry I.
  • The Journal of Chemical Physics, Vol. 138, Issue 19
  • DOI: 10.1063/1.4804164

Equation of motion coupled cluster method for electron attachment
journal, March 1995

  • Nooijen, Marcel; Bartlett, Rodney J.
  • The Journal of Chemical Physics, Vol. 102, Issue 9
  • DOI: 10.1063/1.468592

Effect of microhydration on the electronic structure of the chromophores of the photoactive yellow and green fluorescent proteins
journal, November 2011

  • Zuev, Dmitry; Bravaya, Ksenia B.; Makarova, Maria V.
  • The Journal of Chemical Physics, Vol. 135, Issue 19
  • DOI: 10.1063/1.3660350

Multireference Fock space coupled cluster method in the effective and intermediate Hamiltonian formulation for the (2,0) sector
journal, April 2012

  • Musiał, Monika
  • The Journal of Chemical Physics, Vol. 136, Issue 13
  • DOI: 10.1063/1.3700438

Effect of Protein Environment on Electronically Excited and Ionized States of the Green Fluorescent Protein Chromophore
journal, June 2011

  • Bravaya, Ksenia B.; Khrenova, Maria G.; Grigorenko, Bella L.
  • The Journal of Physical Chemistry B, Vol. 115, Issue 25
  • DOI: 10.1021/jp2020269

Wide-field subdiffraction RESOLFT microscopy using fluorescent protein photoswitching
journal, January 2007

  • A. Schwentker, Miriam; Bock, Hannes; Hofmann, Michael
  • Microscopy Research and Technique, Vol. 70, Issue 3
  • DOI: 10.1002/jemt.20443

Deactivation Pathways of an Isolated Green Fluorescent Protein Model Chromophore Studied by Electronic Action Spectroscopy
journal, December 2009

  • Forbes, Matthew W.; Jockusch, Rebecca A.
  • Journal of the American Chemical Society, Vol. 131, Issue 47
  • DOI: 10.1021/ja9066404

Non-adiabatic dynamics of isolated green fluorescent protein chromophore anion
journal, December 2014

  • Zhao, Li; Zhou, Pan-Wang; Li, Bin
  • The Journal of Chemical Physics, Vol. 141, Issue 23
  • DOI: 10.1063/1.4903241

Active-space completely-renormalized equation-of-motion coupled-cluster formalism: Excited-state studies of green fluorescent protein, free-base porphyrin, and oligoporphyrin dimer
journal, April 2010

  • Kowalski, Karol; Krishnamoorthy, Sriram; Villa, Oreste
  • The Journal of Chemical Physics, Vol. 132, Issue 15
  • DOI: 10.1063/1.3385315
    Sort by:
    [ × clear filter / sort ]

    Works referencing / citing this record:

    Coupled cluster Green function: Model involving single and double excitations
    journal, April 2016

    • Bhaskaran-Nair, Kiran; Kowalski, Karol; Shelton, William A.
    • The Journal of Chemical Physics, Vol. 144, Issue 14
    • DOI: 10.1063/1.4944960
      Sort by:
      [ × clear filter / sort ]

      Similar Records in DOE PAGES and OSTI.GOV collections: