Influence of pump laser fluence on ultrafast myoglobin structural dynamics

Barends, Thomas R. M.; Gorel, Alexander; Bhattacharyya, Swarnendu; Schirò, Giorgio; Bacellar, Camila; Cirelli, Claudio; Colletier, Jacques-Philippe; Foucar, Lutz; Grünbein, Marie Luise; Hartmann, Elisabeth; Hilpert, Mario; Holton, James M.; Johnson, Philip J. M.; Kloos, Marco; Knopp, Gregor; Marekha, Bogdan; Nass, Karol; Kovacs, Gabriela Nass; Ozerov, Dmitry; Stricker, Miriam; Weik, Martin; Doak, R. Bruce; Shoeman, Robert L.; Milne, Christopher J.; Huix-Rotllant, Miquel; Cammarata, Marco; Schlichting, Ilme

doi:10.1038/s41586-024-07032-9

Title: Influence of pump laser fluence on ultrafast myoglobin structural dynamics

Journal Article · 13 February 2024 · Nature (London)

DOI: https://doi.org/10.1038/s41586-024-07032-9 · OSTI ID:2470904

^[1]; Gorel, Alexander ^[1]; Bhattacharyya, Swarnendu ^[2]; Schirò, Giorgio ^[3];

^[4];

^[4]; Colletier, Jacques-Philippe ^[3]; Foucar, Lutz ^[1]; Grünbein, Marie Luise ^[1]; Hartmann, Elisabeth ^[1];

^[1];

^[5];

^[4];

^[6];

^[4]; Marekha, Bogdan ^[7]; Nass, Karol ^[4]; Kovacs, Gabriela Nass ^[1]; Ozerov, Dmitry ^[4]; Stricker, Miriam ^[8] more »

Max Planck Institute for Medical Research, Heidelberg (Germany)
Aix Marseille Univ, Marseille (France)
Université Grenoble Alpes (France)
Paul Scherrer Institute, Villigen (Switzerland)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
European XFEL GmbH, Schenefeld (Germany)
Laboratoire de Chimie UMR, Lyon (France)
University of Oxford (United Kingdom)
ESRF, Grenoble (France)

High-intensity femtosecond pulses from an X-ray free-electron laser enable pump–probe experiments for the investigation of electronic and nuclear changes during light-induced reactions. On timescales ranging from femtoseconds to milliseconds and for a variety of biological systems, time-resolved serial femtosecond crystallography (TR-SFX) has provided detailed structural data for light-induced isomerization, breakage or formation of chemical bonds and electron transfer. However, all ultrafast TR-SFX studies to date have employed such high pump laser energies that nominally several photons were absorbed per chromophore. As multiphoton absorption may force the protein response into non-physiological pathways, it is of great concern whether this experimental approach allows valid conclusions to be drawn vis-à-vis biologically relevant single-photon-induced reactions. Here we describe ultrafast pump–probe SFX experiments on the photodissociation of carboxymyoglobin, showing that different pump laser fluences yield markedly different results. In particular, the dynamics of structural changes and observed indicators of the mechanistically important coherent oscillations of the Fe–CO bond distance (predicted by recent quantum wavepacket dynamics) are seen to depend strongly on pump laser energy, in line with quantum chemical analysis. Our results confirm both the feasibility and necessity of performing ultrafast TR-SFX pump–probe experiments in the linear photoexcitation regime. We consider this to be a starting point for reassessing both the design and the interpretation of ultrafast TR-SFX pump–probe experiments such that mechanistically relevant insight emerges.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; French National Research Agency

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470904

Journal Information:: Nature (London), Journal Name: Nature (London) Journal Issue: 8000 Vol. 626; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (77)

Ultrafast dynamics of myoglobin probed by time‐resolved resonance Raman spectroscopy Mizutani, Yasuhisa; Kitagawa, Teizo The Chemical Record, Vol. 1, Issue 3 https://doi.org/10.1002/tcr.1012	journal	January 2001
Heme Photolysis Occurs by Ultrafast Excited State Metal-to-Ring Charge Transfer Franzen, Stefan; Kiger, Laurent; Poyart, Claude Biophysical Journal, Vol. 80, Issue 5 https://doi.org/10.1016/S0006-3495(01)76207-8	journal	May 2001
Deoxymyoglobin studied by the conformational normal mode analysis Seno, Yasunobu; Gō, Nobuhiro Journal of Molecular Biology, Vol. 216, Issue 1 https://doi.org/10.1016/S0022-2836(05)80063-4	journal	November 1990
Photocycle populations with femtosecond excitation of crystalline photoactive yellow protein Hutchison, Christopher D. M.; Kaucikas, Marius; Tenboer, Jason Chemical Physics Letters, Vol. 654 https://doi.org/10.1016/j.cplett.2016.04.087	journal	June 2016
Addressing high excitation conditions in time-resolved X-ray diffraction experiments and issues of biological relevance Besaw, Jessica E.; Miller, R. J. Dwayne Current Opinion in Structural Biology, Vol. 81 https://doi.org/10.1016/j.sbi.2023.102624	journal	August 2023
High-resolution crystal structures of transient intermediates in the phytochrome photocycle Carrillo, Melissa; Pandey, Suraj; Sanchez, Juan Structure, Vol. 29, Issue 7 https://doi.org/10.1016/j.str.2021.03.004	journal	July 2021
Tinker 8: Software Tools for Molecular Design Rackers, Joshua A.; Wang, Zhi; Lu, Chao Journal of Chemical Theory and Computation, Vol. 14, Issue 10 https://doi.org/10.1021/acs.jctc.8b00529	journal	August 2018
OpenMolcas: From Source Code to Insight Fdez. Galván, Ignacio; Vacher, Morgane; Alavi, Ali Journal of Chemical Theory and Computation, Vol. 15, Issue 11 https://doi.org/10.1021/acs.jctc.9b00532	journal	September 2019
Impact of Ultrafast Electric Field Changes on Photoreceptor Protein Dynamics Heyne, Karsten The Journal of Physical Chemistry B, Vol. 126, Issue 3 https://doi.org/10.1021/acs.jpcb.1c08131	journal	January 2022
Energetics and Dynamics of Deterministic Protein Motion Miller, R. J. Dwayne Accounts of Chemical Research, Vol. 27, Issue 5 https://doi.org/10.1021/ar00041a005	journal	May 1994
Energy Flow from Solute to Solvent Probed by Femtosecond IR Spectroscopy: Malachite Green and Heme Protein Solutions Lian, Tianquan; Locke, Bruce; Kholodenko, Yuriy The Journal of Physical Chemistry, Vol. 98, Issue 45 https://doi.org/10.1021/j100096a005	journal	November 1994
Modeling of Ligation-Induced Helix/Loop Displacements in Myoglobin: Toward an Understanding of Hemoglobin Allostery Guallar, Victor; Jarzecki, Andrzej A.; Friesner, Richard A. Journal of the American Chemical Society, Vol. 128, Issue 16 https://doi.org/10.1021/ja057318h	journal	April 2006
Serial Femtosecond Crystallography Reveals that Photoactivation in a Fluorescent Protein Proceeds via the Hula Twist Mechanism Fadini, Alisia; Hutchison, Christopher D. M.; Morozov, Dmitry Journal of the American Chemical Society, Vol. 145, Issue 29 https://doi.org/10.1021/jacs.3c02313	journal	July 2023
Investigations of Anharmonic Low-Frequency Oscillations in Heme Proteins ^† Rosca, Florin; Kumar, Anand T. N.; Ionascu, Dan The Journal of Physical Chemistry A, Vol. 106, Issue 14 https://doi.org/10.1021/jp0129277	journal	April 2002
Femtosecond Near-IR Absorbance Study of Photoexcited Myoglobin: Dynamics of Electronic and Thermal Relaxation Lim, Manho; Jackson, Timothy A.; Anfinrud, Philip A. The Journal of Physical Chemistry, Vol. 100, Issue 29 https://doi.org/10.1021/jp9536458	journal	January 1996
Femtosecond Heterodyne-Detected Four-Wave-Mixing Studies of Deterministic Protein Motions. 2. Protein Response Goodno, Gregory D.; Astinov, Vladimir; Miller, R. J. Dwayne The Journal of Physical Chemistry A, Vol. 103, Issue 49 https://doi.org/10.1021/jp993559y	journal	November 1999
Structure of a ligand-binding intermediate in wild-type carbonmonoxy myoglobin Chu, Kelvin; Vojtchovský, Jaroslav; McMahon, Benjamin H. Nature, Vol. 403, Issue 6772 https://doi.org/10.1038/35002641	journal	February 2000
Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography Coquelle, Nicolas; Sliwa, Michel; Woodhouse, Joyce Nature Chemistry, Vol. 10, Issue 1 https://doi.org/10.1038/nchem.2853	journal	September 2017
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
CHARMM36m: an improved force field for folded and intrinsically disordered proteins Huang, Jing; Rauscher, Sarah; Nawrocki, Grzegorz Nature Methods, Vol. 14, Issue 1 https://doi.org/10.1038/nmeth.4067	journal	November 2016
Ultrafast carbon monoxide photolysis and heme spin-crossover in myoglobin via nonadiabatic quantum dynamics Falahati, Konstantin; Tamura, Hiroyuki; Burghardt, Irene Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06615-1	journal	October 2018
Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin Nass Kovacs, Gabriela; Colletier, Jacques-Philippe; Grünbein, Marie Luise Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10758-0	journal	July 2019
Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin in the multiphoton regime and biological relevance Miller, R. J. Dwayne; Paré-Labrosse, Olivier; Sarracini, Antoine Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14971-0	journal	March 2020
Structural dynamics in proteins induced by and probed with X-ray free-electron laser pulses Nass, Karol; Gorel, Alexander; Abdullah, Malik M. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15610-4	journal	April 2020
Effect of X-ray free-electron laser-induced shockwaves on haemoglobin microcrystals delivered in a liquid jet Grünbein, Marie Luise; Gorel, Alexander; Foucar, Lutz Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21819-8	journal	March 2021
Watching the release of a photopharmacological drug from tubulin using time-resolved serial crystallography Wranik, Maximilian; Weinert, Tobias; Slavov, Chavdar Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-36481-5	journal	February 2023
Serial crystallography captures dynamic control of sequential electron and proton transfer events in a flavoenzyme Maestre-Reyna, Manuel; Yang, Cheng-Han; Nango, Eriko Nature Chemistry, Vol. 14, Issue 6 https://doi.org/10.1038/s41557-022-00922-3	journal	April 2022
Optical control of ultrafast structural dynamics in a fluorescent protein Hutchison, Christopher D. M.; Baxter, James M.; Fitzpatrick, Ann Nature Chemistry, Vol. 15, Issue 11 https://doi.org/10.1038/s41557-023-01275-1	journal	August 2023
Femtosecond-to-millisecond structural changes in a light-driven sodium pump Skopintsev, Petr; Ehrenberg, David; Weinert, Tobias Nature, Vol. 583, Issue 7815 https://doi.org/10.1038/s41586-020-2307-8	journal	May 2020
Array programming with NumPy Harris, Charles R.; Millman, K. Jarrod; van der Walt, Stéfan J. Nature, Vol. 585, Issue 7825 https://doi.org/10.1038/s41586-020-2649-2	journal	September 2020
Ultrafast structural changes within a photosynthetic reaction centre Dods, Robert; Båth, Petra; Morozov, Dmitry Nature, Vol. 589, Issue 7841, p. 310-314 https://doi.org/10.1038/s41586-020-3000-7	journal	December 2020
Ultrafast structural changes direct the first molecular events of vision Gruhl, Thomas; Weinert, Tobias; Rodrigues, Matthew J. Nature, Vol. 615, Issue 7954 https://doi.org/10.1038/s41586-023-05863-6	journal	March 2023
Author Correction: SciPy 1.0: fundamental algorithms for scientific computing in Python Virtanen, Pauli; Gommers, Ralf; Oliphant, Travis E. Nature Methods, Vol. 17, Issue 3 https://doi.org/10.1038/s41592-020-0772-5	journal	February 2020
Illumination guidelines for ultrafast pump–probe experiments by serial femtosecond crystallography Grünbein, Marie Luise; Stricker, Miriam; Nass Kovacs, Gabriela Nature Methods, Vol. 17, Issue 7 https://doi.org/10.1038/s41592-020-0847-3	journal	May 2020
Growing and making nano- and microcrystals Shoeman, Robert L.; Hartmann, Elisabeth; Schlichting, Ilme Nature Protocols, Vol. 18, Issue 3 https://doi.org/10.1038/s41596-022-00777-5	journal	November 2022
Serial femtosecond crystallography Barends, Thomas R. M.; Stauch, Benjamin; Cherezov, Vadim Nature Reviews Methods Primers, Vol. 2, Issue 1 https://doi.org/10.1038/s43586-022-00141-7	journal	August 2022
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
Theory of vibrational relaxation of polyatomic molecules in liquids Kenkre, V. M.; Tokmakoff, A.; Fayer, M. D. The Journal of Chemical Physics, Vol. 101, Issue 12 https://doi.org/10.1063/1.467876	journal	December 1994
Observing heme doming in myoglobin with femtosecond X-ray absorption spectroscopya) Levantino, M.; Lemke, H. T.; Schirò, G. Structural Dynamics, Vol. 2, Issue 4 https://doi.org/10.1063/1.4921907	journal	May 2015
Modern quantum chemistry with [Open]Molcas Aquilante, Francesco; Autschbach, Jochen; Baiardi, Alberto The Journal of Chemical Physics, Vol. 152, Issue 21 https://doi.org/10.1063/5.0004835	journal	June 2020
Recent developments in the general atomic and molecular electronic structure system Barca, Giuseppe M. J.; Bertoni, Colleen; Carrington, Laura The Journal of Chemical Physics, Vol. 152, Issue 15 https://doi.org/10.1063/5.0005188	journal	April 2020
Interplays of electron and nuclear motions along CO dissociation trajectory in myoglobin revealed by ultrafast X-rays and quantum dynamics calculations Shelby, Megan L.; Wildman, Andrew; Hayes, Dugan Proceedings of the National Academy of Sciences, Vol. 118, Issue 14 https://doi.org/10.1073/pnas.2018966118	journal	March 2021
Early-stage dynamics of chloride ion–pumping rhodopsin revealed by a femtosecond X-ray laser Yun, Ji-Hye; Li, Xuanxuan; Yue, Jianing Proceedings of the National Academy of Sciences, Vol. 118, Issue 13 https://doi.org/10.1073/pnas.2020486118	journal	March 2021
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
Identification of heavy-atom derivatives by normal probability methods Howell, P. L.; Smith, G. D. Journal of Applied Crystallography, Vol. 25, Issue 1 https://doi.org/10.1107/S0021889891010385	journal	February 1992
Indexing in single-crystal diffractometry with an obstinate list of reflections Duisenberg, A. J. M. Journal of Applied Crystallography, Vol. 25, Issue 2 https://doi.org/10.1107/S0021889891010634	journal	April 1992
Structure-factor analysis of femtosecond microdiffraction patterns from protein nanocrystals Kirian, Richard A.; White, Thomas A.; Holton, James M. Acta Crystallographica Section A Foundations of Crystallography, Vol. 67, Issue 2 https://doi.org/10.1107/S0108767310050981	journal	February 2011
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
The integration of macromolecular diffraction data Leslie, Andrew G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1 https://doi.org/10.1107/S0907444905039107	journal	December 2005
Structure-factor extrapolation using the scalar approximation: theory, applications and limitations Genick, Ulrich K. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 10 https://doi.org/10.1107/S0907444907038164	journal	September 2007
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
The CCP4 suite programs for protein crystallography Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
Discerning best practices in XFEL-based biological crystallography – standards for nonstandard experiments Gorel, Alexander; Schlichting, Ilme; Barends, Thomas R. M. IUCrJ, Vol. 8, Issue 4 https://doi.org/10.1107/S205225252100467X	journal	June 2021
XGANDALF – extended gradient descent algorithm for lattice finding Gevorkov, Yaroslav; Yefanov, Oleksandr; Barty, Anton Acta Crystallographica Section A Foundations and Advances, Vol. 75, Issue 5 https://doi.org/10.1107/S2053273319010593	journal	August 2019
Time-resolved serial femtosecond crystallography on fatty-acid photodecarboxylase: lessons learned Hadjidemetriou, Kyprianos; Coquelle, Nicolas; Barends, Thomas R. M. Acta Crystallographica Section D Structural Biology, Vol. 78, Issue 9 https://doi.org/10.1107/S2059798322007525	journal	August 2022
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
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
Structure of a Protein Photocycle Intermediate by Millisecond Time-Resolved Crystallography Genick, U. K. Science, Vol. 275, Issue 5305 https://doi.org/10.1126/science.275.5305.1471	journal	March 1997
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
Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein Pande, K.; Hutchison, C. D. M.; Groenhof, G. Science, Vol. 352, Issue 6286 https://doi.org/10.1126/science.aad5081	journal	May 2016
Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser Nogly, Przemyslaw; Weinert, Tobias; James, Daniel Science https://doi.org/10.1126/science.aat0094	journal	June 2018
Advances and challenges in time-resolved macromolecular crystallography Brändén, Gisela; Neutze, Richard Science, Vol. 373, Issue 6558 https://doi.org/10.1126/science.aba0954	journal	August 2021
Mechanism and dynamics of fatty acid photodecarboxylase Sorigué, D.; Hadjidemetriou, K.; Blangy, S. Science, Vol. 372, Issue 6538 https://doi.org/10.1126/science.abd5687	journal	April 2021
Dynamics and mechanism of a light-driven chloride pump Mous, Sandra; Gotthard, Guillaume; Ehrenberg, David Science, Vol. 375, Issue 6583 https://doi.org/10.1126/science.abj6663	journal	February 2022
Visualizing the DNA repair process by a photolyase at atomic resolution Maestre-Reyna, Manuel; Wang, Po-Hsun; Nango, Eriko Science, Vol. 382, Issue 6674 https://doi.org/10.1126/science.add7795	journal	December 2023
Time-resolved crystallography captures light-driven DNA repair Christou, Nina-Eleni; Apostolopoulou, Virginia; Melo, Diogo V. M. Science, Vol. 382, Issue 6674 https://doi.org/10.1126/science.adj4270	journal	December 2023
X-Ray Free-Electron Lasers for the Structure and Dynamics of Macromolecules Chapman, Henry N. Annual Review of Biochemistry, Vol. 88, Issue 1 https://doi.org/10.1146/annurev-biochem-013118-110744	journal	June 2019
Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography Coquelle, Coquelle Coherent X-ray Imaging Data Bank (Lawrence Berkeley National Laboratory); Institut Laue Langevin https://doi.org/10.11577/1369547	dataset	January 2017
Femtosecond protein nanocrystallography—data analysis methods Kirian, Richard A.; Wang, Xiaoyu; Weierstall, Uwe Optics Express, Vol. 18, Issue 6 https://doi.org/10.1364/OE.18.005713	journal	January 2010
Linear refractive index and absorption measurements of nonlinear optical liquids in the visible and near-infrared spectral region Kedenburg, S.; Vieweg, M.; Gissibl, T. Optical Materials Express, Vol. 2, Issue 11 https://doi.org/10.1364/OME.2.001588	journal	January 2012
Opportunities for Chemistry at the SwissFEL X-ray Free Electron Laser Milne, ChristopherJ.; Beaud, Paul; Deng, Yunpei CHIMIA International Journal for Chemistry, Vol. 71, Issue 5 https://doi.org/10.2533/chimia.2017.299	journal	May 2017
Influence of pump laser fluence on ultrafast myoglobin structural changes Barends, Thomas; Schlichting, Ilme Zenodo https://doi.org/10.5281/zenodo.7341458	dataset	January 2023
Linear refractive index and absorption measurements of nonlinear optical liquids in the visible and near-infrared spectral region Kedenburg, S.; Vieweg, M.; Gissibl, T. Figshare https://doi.org/10.6084/m9.figshare.c.3755522	collection	January 2012
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser Claesson, Elin; Wahlgren, Weixiao Yuan; Takala, Heikki eLife, Vol. 9 https://doi.org/10.7554/eLife.53514	journal	March 2020
Rapid response Hughes, Jon eLife, Vol. 9 https://doi.org/10.7554/eLife.57105	journal	April 2020

Cited By (1)

Influence of pump laser fluence on ultrafast myoglobin structural dynamics Barends, Thomas Coherent X-ray Imaging Data Bank (Lawrence Berkeley National Laboratory); MPI Heidelberg, SwissFEL, PSI https://doi.org/10.11577/2282689	dataset	January 2024

Similar Records

Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography

Journal Article · 2016 · Nature Communications · OSTI ID:1313008

Nogly, Przemyslaw; Panneels, Valerie; Nelson, Garrett; +37 more

Ultrafast nonlinear transparency driven at a telecom wavelength in an organic semiconductor system

Journal Article · 2019 · AIP Advances · OSTI ID:1494938

Park, Joong -Mok; Cheng, Di; Patz, Aaron; +7 more

Femtosecond laser studies of molecular wavepacket dynamics in the cesium dimer

Thesis/Dissertation · 1992 · OSTI ID:7041868

Rodriguez, G

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Molecular biophysics
Nanocrystallography
Science & Technology - Other Topics

Title: Influence of pump laser fluence on ultrafast myoglobin structural dynamics

Citation Formats

References (77)

Cited By (1)

Similar Records

Related Subjects