Femtosecond Crystallography with Ultrabright Electrons and X-rays: Capturing Chemistry in Action

With the recent advances in ultrabright electron and x-ray sources, it is now possible to extend crystallography to the femtosecond time domain to literally light up atomic motions involved in the primary processes governing structural transitions. This review chronicles the development of brighter and brighter electron and x-ray sources that have enabled atomic resolution to structural dynamics for increasingly complex systems. The primary focus is on achieving sufficient brightness using pump-probe protocols to resolve the far-from-equilibrium motions directing chemical processes that in general lead to irreversible changes in samples. Given the central importance of structural transitions to conceptualizing chemistry, this emerging field has the potential to significantly improve our understanding of chemistry and its connection to driving biological processes.

[1]  M. Born.  Thermodynamics of Crystals and Melting , 1939 .

[2]  K. Holmes,et al.  Synchrotron Radiation as a Source for X-ray Diffraction , 1971, Nature.

[3]  V. P. Spiridonov,et al.  A stroboscopical gas-electron diffraction method for the investigation of short-lived molecular species , 1983 .

[4]  Graham R. Fleming,et al.  Chemical applications of ultrafast spectroscopy , 1986 .

[5]  Steven C. Almo,et al.  Time-resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis , 1990, Nature.

[6]  N Go,et al.  Deoxymyoglobin studied by the conformational normal mode analysis. II. The conformational change upon oxygenation. , 1990, Journal of molecular biology.

[7]  R. Miller,et al.  Direct observation of global protein motion in hemoglobin and myoglobin on picosecond time scales. , 1991, Science.

[8]  Ahmed H. Zewail,et al.  Ultrafast diffraction and molecular structure , 1992 .

[9]  A. Zewail,et al.  Ultrafast electron diffraction. Velocity mismatch and temporal resolution in crossed-beam experiments , 1993 .

[10]  R. J. Dwayne Miller,et al.  ENERGETICS AND DYNAMICS OF DETERMINISTIC PROTEIN MOTION , 1994 .

[11]  D Bourgeois,et al.  Photolysis of the Carbon Monoxide Complex of Myoglobin: Nanosecond Time-Resolved Crystallography , 1996, Science.

[12]  Gerard Mourou,et al.  Time-resolved structures of macromolecules at the ESRF: Single-pulse Laue diffraction, stroboscopic data collection and femtosecond flash photolysis , 1997 .

[13]  Patrick Audebert,et al.  Femtosecond time-resolved X-ray diffraction from laser-heated organic films , 1997, Nature.

[14]  Ahmed H. Zewail,et al.  Clocking transient chemical changes by ultrafast electron diffraction , 1997, Nature.

[15]  A. Cavalleri,et al.  Picosecond–milliångström lattice dynamics measured by ultrafast X-ray diffraction , 1999, Nature.

[16]  I. Tomov,et al.  Ultrafast Time-Resolved Transient Structures of Solids and Liquids Studied by Means of X-ray Diffraction and EXAFS , 1999 .

[17]  N. Go,et al.  Investigating protein dynamics in collective coordinate space. , 1999, Current opinion in structural biology.

[18]  W. Leemans,et al.  Ultrafast Structural Dynamics in InSb Probed by Time-Resolved X-Ray Diffraction , 1999 .

[19]  J. Ashby.  References and Notes , 1999 .

[20]  Glover,et al.  Generation of femtosecond pulses of synchrotron radiation , 2000, Science.

[21]  S. Fourmaux,et al.  Non-thermal melting in semiconductors measured at femtosecond resolution , 2001, Nature.

[22]  Peter M. Weber,et al.  Ultrafast Diffraction Imaging of the Electrocyclic Ring-Opening Reaction of 1,3-Cyclohexadiene , 2001 .

[23]  S. Kobatake,et al.  Reversible surface morphology changes of a photochromic diarylethene single crystal by photoirradiation. , 2001, Science.

[24]  H Ihee,et al.  Direct imaging of transient molecular structures with ultrafast diffraction. , 2001, Science.

[25]  A. Cavalleri,et al.  Femtosecond Structural Dynamics in VO2 during an Ultrafast Solid-Solid Phase Transition. , 2001, Physical review letters.

[26]  Jason R. Dwyer,et al.  Ultrafast electron optics: Propagation dynamics of femtosecond electron packets , 2002 .

[27]  R. Miller.  2000 John C. Polanyi Award Lecture Mother Nature and the molecular Big Bang , 2002 .

[28]  S. Subramaniam,et al.  From structure to mechanism: electron crystallographic studies of bacteriorhodopsin , 2002, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[29]  M. Robb,et al.  Can Diarylethene Photochromism Be Explained by a Reaction Path Alone? A CASSCF Study with Model MMVB Dynamics , 2003 .

[30]  S. Techert,et al.  Laser-Induced Ferroelectric Structural Order in an Organic Charge-Transfer Crystal , 2003, Science.

[31]  Aleksandr V. Smirnov,et al.  Watching a Protein as it Functions with 150-ps Time-Resolved X-ray Crystallography , 2003, Science.

[32]  A. Nagy,et al.  Observation of the cascaded atomic-to-global length scales driving protein motion , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Jason R. Dwyer,et al.  An Atomic-Level View of Melting Using Femtosecond Electron Diffraction , 2003, Science.

[34]  R. Henderson.  Realizing the potential of electron cryo-microscopy , 2004, Quarterly Reviews of Biophysics.

[35]  M. Delarue,et al.  On the use of low-frequency normal modes to enforce collective movements in refining macromolecular structural models. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[36]  W. King,et al.  Ultrafast electron microscopy in materials science, biology, and chemistry , 2005 .

[37]  I. Bahar,et al.  Coarse-grained normal mode analysis in structural biology. , 2005, Current opinion in structural biology.

[38]  Zhibin Lin,et al.  Time-resolved diffraction profiles and atomic dynamics in short-pulse laser-induced structural transformations: Molecular dynamics study , 2006 .

[39]  G. Sciara,et al.  Extended subnanosecond structural dynamics of myoglobin revealed by Laue crystallography. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[40]  A. Zewail,et al.  Breaking resolution limits in ultrafast electron diffraction and microscopy , 2006, Proceedings of the National Academy of Sciences.

[41]  Jerome B. Hastings,et al.  Ultrafast Time-Resolved Electron Diffraction with Megavolt Electron Beams , 2006 .

[42]  L. Veisz,et al.  Hybrid dc–ac electron gun for fs-electron pulse generation , 2007 .

[43]  T Schmidt,et al.  Spatiotemporal stability of a femtosecond hard-x-ray undulator source studied by control of coherent optical phonons. , 2007, Physical review letters.

[44]  Canada.,et al.  Electron source concept for single-shot sub-100 fs electron diffraction in the 100 keV range , 2007, physics/0702018.

[45]  J. Echave,et al.  Evolutionary conservation of protein vibrational dynamics. , 2008, Gene.

[46]  Maher Harb,et al.  Grating enhanced ponderomotive scattering for visualization and full characterization of femtosecond electron pulses. , 2008, Optics express.

[47]  M. Lagally,et al.  Electronically driven structure changes of Si captured by femtosecond electron diffraction. , 2008, Physical review letters.

[48]  R. Miller,et al.  Electronic acceleration of atomic motions and disordering in bismuth , 2009, Nature.

[49]  M. Messerschmidt,et al.  The RATIO method for time-resolved Laue crystallography. , 2009, Journal of synchrotron radiation.

[50]  S. Johnson,et al.  Full reconstruction of a crystal unit cell structure during coherent femtosecond motion. , 2009, Physical review letters.

[51]  R. J. Dwayne Miller,et al.  The Formation of Warm Dense Matter: Experimental Evidence for Electronic Bond Hardening in Gold , 2009, Science.

[52]  Renkai Li,et al.  Capturing ultrafast structural evolutions with a single pulse of MeV electrons: Radio frequency streak camera based electron diffraction , 2010 .

[53]  D. Ratner,et al.  First lasing and operation of an ångstrom-wavelength free-electron laser , 2010 .

[54]  T. Elsaesser,et al.  Concerted electron and proton transfer in ionic crystals mapped by femtosecond x-ray powder diffraction. , 2010, The Journal of chemical physics.

[55]  R. J. Dwayne Miller,et al.  Ultrafast Mid-IR Laser Scalpel: Protein Signals of the Fundamental Limits to Minimally Invasive Surgery , 2010, PloS one.

[56]  R. Miller,et al.  Snapshots of cooperative atomic motions in the optical suppression of charge density waves , 2010, Nature.

[57]  F. Krausz,et al.  Single-electron pulses for ultrafast diffraction , 2010, Proceedings of the National Academy of Sciences.

[58]  M. Messerschmidt,et al.  Time-resolved synchrotron diffraction and theoretical studies of very short-lived photo-induced molecular species. , 2010, Acta crystallographica. Section A, Foundations of crystallography.

[59]  T. Elsaesser,et al.  Photoinduced structural dynamics of polar solids studied by femtosecond X-ray diffraction. , 2010, Acta crystallographica. Section A, Foundations of crystallography.

[60]  Germán Sciaini,et al.  Femtosecond electron diffraction: heralding the era of atomically resolved dynamics , 2011 .

[61]  Self-localizing stabilized mega-pixel picoliter arrays with size-exclusion sorting capabilities. , 2011, Analytical chemistry.

[62]  Jinfeng Yang,et al.  Transmission-electron diffraction by MeV electron pulses , 2011 .

[63]  R. R. Cooney,et al.  Femtosecond dynamics of the ring closing process of diarylethene: a case study of electrocyclic reactions in photochromic single crystals. , 2011, The journal of physical chemistry. A.

[64]  S. Johnson,et al.  Nonthermal melting of a charge density wave in TiSe2. , 2011, Physical review letters.

[65]  D. Yarkony,et al.  Role of conical intersections in molecular spectroscopy and photoinduced chemical dynamics. , 2012, Annual review of physical chemistry.

[66]  A. Zarrine-Afsar,et al.  Crystallography on a chip. , 2012, Acta crystallographica. Section D, Biological crystallography.

[67]  Ville R. I. Kaila,et al.  Watching a signaling protein function in real time via 100-ps time-resolved Laue crystallography , 2012, Proceedings of the National Academy of Sciences.

[68]  Structural dynamics of two-dimensional charge-density waves in CeTe 3 investigated by ultrafast electron crystallography , 2012 .

[69]  Philip Coppens,et al.  Ultrafast spin-state photoswitching in a crystal and slower consecutive processes investigated by femtosecond optical spectroscopy and picosecond X-ray diffraction. , 2012, Physical chemistry chemical physics : PCCP.

[70]  J. Demšar,et al.  Ultrafast dynamics of charge density waves in 4H(b)-TaSe2 probed by femtosecond electron diffraction. , 2012, Physical review letters.

[71]  U Weierstall,et al.  X-ray lasers for structural and dynamic biology , 2012, Reports on progress in physics. Physical Society.

[72]  Georg Weidenspointner,et al.  Time-resolved protein nanocrystallography using an X-ray free-electron laser , 2012, Optics express.

[73]  R. R. Cooney,et al.  Ring-closing reaction in diarylethene captured by femtosecond electron crystallography. , 2013, The journal of physical chemistry. B.

[74]  Anton Barty,et al.  Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser , 2013, Science.

[75]  T. Elsaesser,et al.  Field-driven dynamics of correlated electrons in LiH and NaBH4 revealed by femtosecond x-ray diffraction. , 2013, Physical review letters.

[76]  R. Miller,et al.  Single shot time stamping of ultrabright radio frequency compressed electron pulses , 2013 .

[77]  R. R. Cooney,et al.  Mapping molecular motions leading to charge delocalization with ultrabright electrons , 2013, Nature.

[78]  Judith A K Howard,et al.  Cutting-Edge Techniques Used for the Structural Investigation of Single Crystals , 2014, Science.

[79]  Elspeth F. Garman,et al.  Developments in X-ray Crystallographic Structure Determination of Biological Macromolecules , 2014, Science.

[80]  R. Miller,et al.  Mapping atomic motions with ultrabright electrons: the chemists' gedanken experiment enters the lab frame. , 2014, Annual review of physical chemistry.