Feasibilityof imaging living cells at subnanometer resolutionsbyultrafastX-raydiffraction

Detailed structural investigations on living cells are problematic because existing structural methods cannot reach high resolutions on non-reproducible objects. Illumination with an ultrashort and extremely bright X-ray pulse can outrun key damage processes over a very short period. This can be exploited to extend the diffraction signal to the highest possible resolution in flash diffraction experiments. Here we present an analysis of the interaction of a very intense and very short X-ray pulse with a living cell, using a non-equilibrium population kinetics plasma code with radiation transfer. Each element in the evolving plasma is modeled by numerous states to monitor changes in the atomic populations as a function of pulse length, wavelength, and fluence. The model treats photoionization, impact ionization, Auger decay, recombination, and inverse bremsstrahlung by solving rate equations in a self-consistent manner and describes hydrodynamic expansion through the ion sound speed. The results show that subnanometer resolutions could be reached on micron-sized cells in a diffractionlimited geometry at wavelengths between 0 75 and 1 5 nm and at fluences of 10–10 photons mm in less than 10 fs. Subnanometer resolutions could also be achieved with harder X-rays at higher fluences. We discuss experimental and computational strategies to obtain depth information about the object in flash diffraction experiments.

[1]  P. Debye,et al.  Interferenz von Röntgenstrahlen und Wärmebewegung , 1913 .

[2]  Ivar Waller,et al.  Zur Frage der Einwirkung der Wärmebewegung auf die Interferenz von Röntgenstrahlen , 1923 .

[3]  D. Sayre.  Some implications of a theorem due to Shannon , 1952 .

[4]  W. Leyko,et al.  [Structure of haemoglobin]. , 1960, Postepy biochemii.

[5]  John C. Stewart,et al.  Lowering of Ionization Potentials in Plasmas , 1966 .

[6]  W A Hendrickson,et al.  Radiation damage in protein crystallography. , 1976, Journal of molecular biology.

[7]  T. M. Cannon,et al.  Coded aperture imaging with uniformly redundant arrays. , 1978, Applied optics.

[8]  E E Fenimore,et al.  Tomographical imaging using uniformly redundant arrays. , 1979, Applied optics.

[9]  Richard M. More,et al.  Electronic energy-levels in dense plasmas , 1982 .

[10]  J. Solem,et al.  Microholography of Living Organisms , 1982, Science.

[11]  A. Zamyatnin,et al.  Amino acid, peptide, and protein volume in solution. , 1984, Annual review of biophysics and bioengineering.

[12]  J. W. Campbell,et al.  Millisecond X-ray diffraction and the first electron density map from Laue photographs of a protein crystal , 1987, Nature.

[13]  M. Rosen,et al.  Wavelength choice for soft x-ray laser holography of biological samples. , 1989, Applied optics.

[14]  Richard H. Sherman,et al.  Chaotic communications in the presence of noise , 1993, Optics & Photonics.

[15]  B. L. Henke,et al.  X-Ray Interactions: Photoabsorption, Scattering, Transmission, and Reflection at E = 50-30,000 eV, Z = 1-92 , 1993 .

[16]  H. Scott,et al.  GLF - A simulation code for X-ray lasers , 1994 .

[17]  R. Henderson.  The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules , 1995, Quarterly Reviews of Biophysics.

[18]  J. Miao,et al.  Phase retrieval from the magnitude of the Fourier transforms of nonperiodic objects , 1998 .

[19]  M. Heel,et al.  Single-particle electron cryo-microscopy: towards atomic resolution , 2000, Quarterly Reviews of Biophysics.

[20]  J. Hajdu,et al.  Potential for biomolecular imaging with femtosecond X-ray pulses , 2000, Nature.

[21]  Howard A. Scott,et al.  Cretin—a radiative transfer capability for laboratory plasmas , 2001 .

[22]  M. Howells,et al.  Phase recovery and lensless imaging by iterative methods in optical, X-ray and electron diffraction , 2002, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[23]  J. Hajdu,et al.  Diffraction imaging of single particles and biomolecules. , 2003, Journal of structural biology.

[24]  J. Cary,et al.  High-quality electron beams from a laser wakefield accelerator using plasma-channel guiding , 2004, Nature.

[25]  Carl Caleman,et al.  Auger electron cascades in water and ice , 2004 .

[26]  Gyula Faigel,et al.  Dynamics in a cluster under the influence of intense femtosecond hard X-ray pulses , 2004 .

[27]  Qun Shen,et al.  Diffractive imaging of nonperiodic materials with future coherent X-ray sources. , 2004, Journal of synchrotron radiation.

[28]  Plasmas with an index of refraction greater than 1. , 2004, Optics letters.

[29]  Y. Glinec,et al.  A laser–plasma accelerator producing monoenergetic electron beams , 2004, Nature.

[30]  Imaging atom clusters by hard X-ray free-electron lasers , 2003, cond-mat/0309083.

[31]  Abraham Szoke,et al.  Dynamics of biological molecules irradiated by short x-ray pulses. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[32]  R. London,et al.  Pulse requirements for x-ray diffraction imaging of single biological molecules. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  J. Frank.  Three-Dimensional Electron Microscopy of Macromolecular Assemblies , 2006 .

[34]  D. Sayre,et al.  Electronic Reprint Foundations of Crystallography Reconstruction of a Yeast Cell from X-ray Diffraction Data Foundations of Crystallography Reconstruction of a Yeast Cell from X-ray Diffraction Data , 2022 .

[35]  M. D. de Jonge,et al.  Fresnel coherent diffractive imaging. , 2006, Physical review letters.

[36]  W. H. Benner,et al.  Femtosecond diffractive imaging with a soft-X-ray free-electron laser , 2006, physics/0610044.

[37]  P. Nicolosi,et al.  First operation of a free-electron laser generating GW power radiation at 32 nm wavelength , 2006 .

[38]  S. Marchesini,et al.  High-resolution ab initio three-dimensional x-ray diffraction microscopy. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[39]  D. Paterson,et al.  Diffractive imaging of highly focused X-ray fields , 2006 .

[40]  Richard A. London,et al.  Femtosecond time-delay X-ray holography , 2007, Nature.

[41]  M. Ferrario,et al.  Design considerations for table-top, laser-based VUV and X-ray free electron lasers , 2007 .

[42]  R. London,et al.  Encapsulation and diffraction-pattern-correction methods to reduce the effect of damage in x-ray diffraction imaging of single biological molecules. , 2007, Physical review letters.

[43]  G. Hasinger,et al.  Fast large-area spectroscopic and imaging CCD detectors for x-ray astronomy with eROSITA and for exploration of the nanocosmos , 2007, SPIE Optical Engineering + Applications.

[44]  G Bortel,et al.  Classification of continuous diffraction patterns: a numerical study. , 2007, Journal of structural biology.

[45]  U Weierstall,et al.  Dose, exposure time and resolution in serial X-ray crystallography. , 2007, Journal of synchrotron radiation.

[46]  Garth J. Williams,et al.  Keyhole coherent diffractive imaging , 2008 .

[47]  Joshua W. Shaevitz,et al.  Massively parallel X-ray holography , 2008 .

[48]  J. Kirz,et al.  An assessment of the resolution limitation due to radiation-damage in x-ray diffraction microscopy. , 2005, Journal of Electron Spectroscopy and Related Phenomena.