Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein

Pande, K.; Hutchison, C. D. M.; Groenhof, G.; Aquila, A.; Robinson, J. S.; Tenboer, J.; Basu, S.; Boutet, S.; DePonte, D. P.; Liang, M.; White, T. A.; Zatsepin, N. A.; Yefanov, O.; Morozov, D.; Oberthuer, D.; Gati, C.; Subramanian, G.; James, D.; Zhao, Y.; Koralek, J.; Brayshaw, J.; Kupitz, C.; Conrad, C.; Roy-Chowdhury, S.; Coe, J. D.; Metz, M.; Xavier, P. L.; Grant, T. D.; Koglin, J. E.; Ketawala, G.; Fromme, R.; rajer, V.; Henning, R.; Spence, J. C. H.; Ourmazd, A.; Schwander, P.; Weierstall, U.; Frank, M.; Fromme, P.; Barty, A.; Chapman, H. N.; Moffat, K.; van Thor, J. J.; Schmidt, M.

doi:10.1126/science.aad5081

Title: Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein

Journal Article · Thu May 05 00:00:00 EDT 2016 · Science

DOI:https://doi.org/10.1126/science.aad5081· OSTI ID:1355852

Pande, K.; Hutchison, C. D. M.; Groenhof, G.; Aquila, A.; Robinson, J. S.; Tenboer, J.; Basu, S.; Boutet, S.; DePonte, D. P.; Liang, M.; White, T. A.; Zatsepin, N. A.; Yefanov, O.; Morozov, D.; Oberthuer, D.; Gati, C.; Subramanian, G.; James, D.; Zhao, Y.; Koralek, J. more »

A variety of organisms have evolved mechanisms to detect and respond to light, in which the response is mediated by protein structural changes following photon absorption. The initial step is often the photo-isomerization of a conjugated chromophore. Furthermore, isomerization occurs on ultrafast timescales and is substantially influenced by the chromophore environment. Here we identify structural changes associated with the earliest steps in the trans to cis isomerization of the chromophore in photoactive yellow protein. Femtosecond, hard X-ray pulses emitted by the Linac Coherent Light Source were used to conduct time-resolved serial femtosecond crystallography on PYP microcrystals over the time range from 100 femtoseconds to 3 picoseconds to determine the structural dynamics of the photoisomerization reaction.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Laboratory Directed Research and Development (LDRD) Program; National Science Foundation (NSF); National Institutes of Health (NIH); Federal Ministry of Education and Research (BMBF)

Grant/Contract Number:: AC52-07NA27344; AC02-76SF00515; 012-ERD-031; NSF-1231306; NSF-0952643; NSF-1158138; R01GM095583; R01EY024363; R24GM111072; P41GM103393; 05K14CHA

OSTI ID:: 1355852

Alternate ID(s):: OSTI ID: 2229607

Report Number(s):: LLNL-JRNL-857679; 352/6286/725

Journal Information:: Science, Journal Name: Science Vol. 352 Journal Issue: 6286; ISSN 0036-8075

Publisher:: American Association for the Advancement of Science (AAAS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 289 works

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References (78)

Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data Barty, Anton; Kirian, Richard A.; Maia, Filipe R. N. C. Journal of Applied Crystallography, Vol. 47, Issue 3 https://doi.org/10.1107/S1600576714007626	journal	May 2014
CrystFEL : a software suite for snapshot serial crystallography White, Thomas A.; Kirian, Richard A.; Martin, Andrew V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812002312	journal	March 2012
Time-resolved Laue diffraction of excited species at atomic resolution: 100 ps single-pulse diffraction of the excited state of the organometallic complex Rh2(μ-PNP)2(PNP)2·BPh4 Benedict, Jason B.; Makal, Anna; Sokolow, Jesse D. Chemical Communications, Vol. 47, Issue 6 https://doi.org/10.1039/c0cc04997b	journal	January 2011
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Photoisomerization and Photoionization of the Photoactive Yellow Protein Chromophore in Solution Larsen, Delmar S.; Vengris, Mikas; van Stokkum, Ivo H. M. Biophysical Journal, Vol. 86, Issue 4 https://doi.org/10.1016/S0006-3495(04)74309-X	journal	April 2004
Time-resolved pump-probe experiments at the LCLS Glownia, James M.; Cryan, J.; Andreasson, J. Optics Express, Vol. 18, Issue 17 https://doi.org/10.1364/OE.18.017620	journal	January 2010
The hydration shell of myoglobin Parak, F.; Hartmann, H.; Schmidt, M. European Biophysics Journal, Vol. 21, Issue 5 https://doi.org/10.1007/BF00188343	journal	November 1992
GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation Hess, Berk; Kutzner, Carsten; van der Spoel, David Journal of Chemical Theory and Computation, Vol. 4, Issue 3 https://doi.org/10.1021/ct700301q	journal	February 2008
Mapping molecular motions leading to charge delocalization with ultrabright electrons Gao, Meng; Lu, Cheng; Jean-Ruel, Hubert Nature, Vol. 496, Issue 7445 https://doi.org/10.1038/nature12044	journal	April 2013
Approximate switching algorithms for trajectory surface hopping Fabiano, E.; Groenhof, G.; Thiel, W. Chemical Physics, Vol. 351, Issue 1-3 https://doi.org/10.1016/j.chemphys.2008.04.003	journal	July 2008
Spectroscopic Studies of Model Photo-Receptors: Validation of a Nanosecond Time-Resolved Micro-Spectrophotometer Design Using Photoactive Yellow Protein and α-Phycoerythrocyanin Purwar, Namrta; Tenboer, Jason; Tripathi, Shailesh International Journal of Molecular Sciences, Vol. 14, Issue 9 https://doi.org/10.3390/ijms140918881	journal	September 2013
GROMACS: Fast, flexible, and free Van Der Spoel, David; Lindahl, Erik; Hess, Berk Journal of Computational Chemistry, Vol. 26, Issue 16 https://doi.org/10.1002/jcc.20291	journal	January 2005
Coherent oscillations in ultrafast fluorescence of photoactive yellow protein Nakamura, Ryosuke; Hamada, Norio; Ichida, Hideki The Journal of Chemical Physics, Vol. 127, Issue 21 https://doi.org/10.1063/1.2802297	journal	December 2007
Contrasting the Excited-State Dynamics of the Photoactive Yellow Protein Chromophore: Protein versus Solvent Environments Vengris, Mikas; van der Horst, Michael A.; Zgrablić, Goran Biophysical Journal, Vol. 87, Issue 3 https://doi.org/10.1529/biophysj.104.043224	journal	September 2004
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Injector for scattering measurements on fully solvated biospecies Weierstall, U.; Spence, J. C. H.; Doak, R. B. Review of Scientific Instruments, Vol. 83, Issue 3 https://doi.org/10.1063/1.3693040	journal	March 2012
Sub-femtosecond precision measurement of relative X-ray arrival time for free-electron lasers Hartmann, N.; Helml, W.; Galler, A. Nature Photonics, Vol. 8, Issue 9 https://doi.org/10.1038/nphoton.2014.164	journal	July 2014
A new mixing of Hartree–Fock and local density‐functional theories Becke, Axel D. The Journal of Chemical Physics, Vol. 98, Issue 2 https://doi.org/10.1063/1.464304	journal	January 1993
Bicycle-pedal model for the first step in the vision process Warshel, Arieh Nature, Vol. 260, Issue 5553 https://doi.org/10.1038/260679a0	journal	April 1976
Frequency-resolved optical gating and single-shot spectral measurements reveal fine structure in microstructure-fiber continuum Gu, Xun; Xu, Lin; Kimmel, Mark Optics Letters, Vol. 27, Issue 13 https://doi.org/10.1364/OL.27.001174	journal	January 2002
Molecular Basis of Visual Excitation Wald, G. Science, Vol. 162, Issue 3850 https://doi.org/10.1126/science.162.3850.230	journal	October 1968
Ultrafast photoinduced reaction dynamics of photoactive yellow protein (PYP): observation of coherent oscillations in the femtosecond fluorescence decay dynamics Mataga, Noboru; Chosrowjan, Haik; Shibata, Yutaka Chemical Physics Letters, Vol. 352, Issue 3-4 https://doi.org/10.1016/S0009-2614(01)01448-8	journal	January 2002
Femtosecond Spectroscopic Observations of Initial Intermediates in the Photocycle of the Photoactive Yellow Protein from Ectothiorhodospira halophila Devanathan, Savitha; Pacheco, Andrew; Ujj, Laszlo Biophysical Journal, Vol. 77, Issue 2 https://doi.org/10.1016/S0006-3495(99)76952-3	journal	August 1999
Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein Tenboer, Jason; Basu, Shibom; Zatsepin, Nadia Science, Vol. 346, Issue 6214 https://doi.org/10.1126/science.1259357	journal	December 2014
Visualizing Photochemical Dynamics in Solution through Picosecond X-Ray Scattering Neutze, Richard; Wouts, Remco; Techert, Simone Physical Review Letters, Vol. 87, Issue 19 https://doi.org/10.1103/PhysRevLett.87.195508	journal	October 2001
Volume-conserving trans–cis isomerization pathways in photoactive yellow protein visualized by picosecond X-ray crystallography Jung, Yang Ouk; Lee, Jae Hyuk; Kim, Joonghan Nature Chemistry, Vol. 5, Issue 3 https://doi.org/10.1038/nchem.1565	journal	February 2013
Excited-state structure by time-resolved X-ray diffraction Kim, Christopher D.; Pillet, Sebastien; Wu, Guang Acta Crystallographica Section A Foundations of Crystallography, Vol. 58, Issue 2 https://doi.org/10.1107/S0108767301017986	journal	February 2002
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Quantum Mechanical Continuum Solvation Models Tomasi, Jacopo; Mennucci, Benedetta; Cammi, Roberto Chemical Reviews, Vol. 105, Issue 8 https://doi.org/10.1021/cr9904009	journal	August 2005
Selective Excitation of Vibrational Wave Packet Motion Using Chirped Pulses Bardeen, C. J.; Wang, Q.; Shank, C. V. Physical Review Letters, Vol. 75, Issue 19 https://doi.org/10.1103/PhysRevLett.75.3410	journal	November 1995
Ultrafast X-ray Diffraction of Transient Molecular Structures in Solution Ihee, H. Science, Vol. 309, Issue 5738 https://doi.org/10.1126/science.1114782	journal	August 2005
Post-refinement method for snapshot serial crystallography White, Thomas A. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0330	journal	July 2014
Femtochemistry: Atomic-Scale Dynamics of the Chemical Bond Using Ultrafast Lasers (Nobel Lecture) Zewail, Ahmed H. Angewandte Chemie International Edition, Vol. 39, Issue 15, p. 2586-2631 https://doi.org/10.1002/1521-3773(20000804)39:15<2586::AID-ANIE2586>3.0.CO;2-O	journal	August 2000
From The Cover: Visualizing reaction pathways in photoactive yellow protein from nanoseconds to seconds Ihee, H.; Rajagopal, S.; Srajer, V. Proceedings of the National Academy of Sciences, Vol. 102, Issue 20 https://doi.org/10.1073/pnas.0409035102	journal	May 2005
Extended multi-configuration quasi-degenerate perturbation theory: The new approach to multi-state multi-reference perturbation theory Granovsky, Alexander A. The Journal of Chemical Physics, Vol. 134, Issue 21 https://doi.org/10.1063/1.3596699	journal	June 2011
Photoisomerisation quantum yield and non-linear cross-sections with femtosecond excitation of the photoactive yellow protein Lincoln, Craig N.; Fitzpatrick, Ann E.; Thor, Jasper J. van Physical Chemistry Chemical Physics, Vol. 14, Issue 45 https://doi.org/10.1039/c2cp41718a	journal	January 2012
A complete active space SCF method (CASSCF) using a density matrix formulated super-CI approach Roos, Björn O.; Taylor, Peter R.; Sigbahn, Per E. M. Chemical Physics, Vol. 48, Issue 2 https://doi.org/10.1016/0301-0104(80)80045-0	journal	May 1980
Photoactivation of the Photoactive Yellow Protein: Why Photon Absorption Triggers a Trans-to-Cis Isomerization of the Chromophore in the Protein Groenhof, Gerrit; Bouxin-Cademartory, Mathieu; Hess, Berk Journal of the American Chemical Society, Vol. 126, Issue 13 https://doi.org/10.1021/ja039557f	journal	April 2004
Application of Singular Value Decomposition to the Analysis of Time-Resolved Macromolecular X-Ray Data Schmidt, Marius; Rajagopal, Sudarshan; Ren, Zhong Biophysical Journal, Vol. 84, Issue 3 https://doi.org/10.1016/S0006-3495(03)75018-8	journal	March 2003
Canonical sampling through velocity rescaling Bussi, Giovanni; Donadio, Davide; Parrinello, Michele The Journal of Chemical Physics, Vol. 126, Issue 1 https://doi.org/10.1063/1.2408420	journal	January 2007
Watching a signaling protein function in real time via 100-ps time-resolved Laue crystallography Schotte, F.; Cho, H. S.; Kaila, V. R. I. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1210938109	journal	November 2012
Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Lee, Chengteh; Yang, Weitao; Parr, Robert G. Physical Review B, Vol. 37, Issue 2 https://doi.org/10.1103/PhysRevB.37.785	journal	January 1988
LINCS: A linear constraint solver for molecular simulations Hess, Berk; Bekker, Henk; Berendsen, Herman J. C. Journal of Computational Chemistry, Vol. 18, Issue 12 https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H	journal	September 1997
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
Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser Arnlund, David; Johansson, Linda C.; Wickstrand, Cecilia Nature Methods, Vol. 11, Issue 9 https://doi.org/10.1038/nmeth.3067	journal	August 2014
Control of selectivity of chemical reaction via control of wave packet evolution Tannor, David J.; Rice, Stuart A. The Journal of Chemical Physics, Vol. 83, Issue 10, p. 5013-5018 https://doi.org/10.1063/1.449767	journal	November 1985
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Quantum model simulation of complete S0→S1 population transfer by means of intense laser pulses with opposite chirp Manz, J.; Naundorf, H.; Yamashita, K. The Journal of Chemical Physics, Vol. 113, Issue 20 https://doi.org/10.1063/1.1319347	journal	November 2000
Ultrafast myoglobin structural dynamics observed with an X-ray free-electron laser Levantino, Matteo; Schirò, Giorgio; Lemke, Henrik Till Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7772	journal	April 2015
Force Spectroscopy of Single Biomolecules Rief, Matthias; Grubmüller, Helmut ChemPhysChem, Vol. 3, Issue 3 https://doi.org/10.1002/1439-7641(20020315)3:3<255::AID-CPHC255>3.0.CO;2-M	journal	March 2002
Use of Non-crystallographic Symmetry in Protein Structure Refinement Kleywegt, G. J. Acta Crystallographica Section D Biological Crystallography, Vol. 52, Issue 4 https://doi.org/10.1107/S0907444995016477	journal	July 1996
Direct Observation of Cooling of Heme Upon Photodissociation of Carbonmonoxy Myoglobin Mizutani, Y. Science, Vol. 278, Issue 5337 https://doi.org/10.1126/science.278.5337.443	journal	October 1997
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
The CSPAD megapixel x-ray camera at LCLS Hart, Philip; Boutet, Sébastien; Carini, Gabriella SPIE Optical Engineering + Applications, SPIE Proceedings https://doi.org/10.1117/12.930924	conference	October 2012
Investigations of ultrafast nuclear response induced by resonant and nonresonant laser pulses Kumar, Anand T. N.; Rosca, Florin; Widom, Allan The Journal of Chemical Physics, Vol. 114, Issue 15 https://doi.org/10.1063/1.1356011	journal	April 2001
Application of chirped ultrashort pulses for generating large-amplitude ground-state vibrational coherence: a computer simulation Ruhman, S.; Kosloff, R. Journal of the Optical Society of America B, Vol. 7, Issue 8 https://doi.org/10.1364/JOSAB.7.001748	journal	January 1990
Myoglobin Dynamics Measured With Vibrational Echo Experiments Rector, K. D.; Fayer, M. D. Laser Chemistry, Vol. 19, Issue 1-4 https://doi.org/10.1155/1999/83895	journal	January 1999
The interpretation of protein structures: Estimation of static accessibility Lee, B.; Richards, F. M. Journal of Molecular Biology, Vol. 55, Issue 3 https://doi.org/10.1016/0022-2836(71)90324-X	journal	February 1971
Solvent cage effects and chemical dynamics in liquids Patron, Francis; Adelman, Steven A. Chemical Physics, Vol. 152, Issue 1-2 https://doi.org/10.1016/0301-0104(91)80039-K	journal	April 1991
Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models Miyamoto, Shuichi; Kollman, Peter A. Journal of Computational Chemistry, Vol. 13, Issue 8 https://doi.org/10.1002/jcc.540130805	journal	October 1992
Initial Steps of Signal Generation in Photoactive Yellow Protein Revealed with Femtosecond Mid-Infrared Spectroscopy ^† Groot, Marie Louise; van Wilderen, Luuk J. G. W.; Larsen, Delmar S. Biochemistry, Vol. 42, Issue 34 https://doi.org/10.1021/bi034878p	journal	September 2003
Picosecond X-Ray Diffraction Probed Transient Structural Changes in Organic Solids Techert, S.; Schotte, F.; Wulff, M. Physical Review Letters, Vol. 86, Issue 10 https://doi.org/10.1103/PhysRevLett.86.2030	journal	March 2001
Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions Brown, Alan; Long, Fei; Nicholls, Robert A. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 1 https://doi.org/10.1107/S1399004714021683	journal	January 2015
Direct observation of global protein motion in hemoglobin and myoglobin on picosecond time scales Genberg, L.; Richard, L.; McLendon, G. Science, Vol. 251, Issue 4997 https://doi.org/10.1126/science.1998121	journal	March 1991
Structural Evolution of the Chromophore in the Primary Stages of Trans/Cis Isomerization in Photoactive Yellow Protein Heyne, Karsten; Mohammed, Omar F.; Usman, Anwar Journal of the American Chemical Society, Vol. 127, Issue 51 https://doi.org/10.1021/ja051210k	journal	December 2005
Spectral encoding of x-ray/optical relative delay Bionta, Mina R.; Lemke, H. T.; Cryan, J. P. Optics Express, Vol. 19, Issue 22 https://doi.org/10.1364/OE.19.021855	journal	January 2011
Photochemical reactions in biological systems: probing the effect of the environment by means of hybrid quantum chemistry/molecular mechanics simulations Boggio-Pasqua, Martial; Burmeister, Carl F.; Robb, Michael A. Physical Chemistry Chemical Physics, Vol. 14, Issue 22 https://doi.org/10.1039/c2cp23628a	journal	January 2012
Protein energy landscapes determined by five-dimensional crystallography Schmidt, Marius; Srajer, Vukica; Henning, Robert Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 12 https://doi.org/10.1107/S0907444913025997	journal	November 2013
3V: cavity, channel and cleft volume calculator and extractor Voss, N. R.; Gerstein, M. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq395	journal	May 2010
A smooth particle mesh Ewald method Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L. The Journal of Chemical Physics, Vol. 103, Issue 19 https://doi.org/10.1063/1.470117	journal	November 1995
CHEMISTRY: Following the Flow of Energy in Biomolecules Champion, P. M. Science, Vol. 310, Issue 5750 https://doi.org/10.1126/science.1120280	journal	November 2005
A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations Duan, Yong; Wu, Chun; Chowdhury, Shibasish Journal of Computational Chemistry, Vol. 24, Issue 16 https://doi.org/10.1002/jcc.10349	journal	October 2003
The Protein Data Bank Berman, Helen M.; Battistuz, Tammy; Bhat, T. N. Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 6 https://doi.org/10.1107/S0907444902003451	journal	May 2002
Measuring ultrashort laser pulses in the time-frequency domain using frequency-resolved optical gating Trebino, Rick; DeLong, Kenneth W.; Fittinghoff, David N. Review of Scientific Instruments, Vol. 68, Issue 9, p. 3277-3295 https://doi.org/10.1063/1.1148286	journal	September 1997
Incoherent Manipulation of the Photoactive Yellow Protein Photocycle with Dispersed Pump-Dump-Probe Spectroscopy Larsen, Delmar S.; van Stokkum, Ivo H. M.; Vengris, Mikas Biophysical Journal, Vol. 87, Issue 3 https://doi.org/10.1529/biophysj.104.043794	journal	September 2004
Chromophore Dynamics in the PYP Photocycle from Femtosecond Stimulated Raman Spectroscopy Creelman, Mark; Kumauchi, Masato; Hoff, Wouter D. The Journal of Physical Chemistry B, Vol. 118, Issue 3 https://doi.org/10.1021/jp408584v	journal	January 2014
Ultrafast infrared spectroscopy reveals a key step for successful entry into the photocycle for photoactive yellow protein van Wilderen, L. J. G. W.; van der Horst, M. A.; van Stokkum, I. H. M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 41 https://doi.org/10.1073/pnas.0603476103	journal	October 2006
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation Barends, T. R. M.; Foucar, L.; Ardevol, A. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac5492	journal	September 2015

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