Abstract
Ultrafast X-ray imaging on individual fragile specimens such as aerosols1, metastable particles2, superfluid quantum systems3 and live biospecimens4 provides high-resolution information that is inaccessible with conventional imaging techniques. Coherent X-ray diffractive imaging, however, suffers from intrinsic loss of phase, and therefore structure recovery is often complicated and not always uniquely defined4,5. Here, we introduce the method of in-flight holography, where we use nanoclusters as reference X-ray scatterers to encode relative phase information into diffraction patterns of a virus. The resulting hologram contains an unambiguous three-dimensional map of a virus and two nanoclusters with the highest lateral resolution so far achieved via single shot X-ray holography. Our approach unlocks the benefits of holography for ultrafast X-ray imaging of nanoscale, non-periodic systems and paves the way to direct observation of complex electron dynamics down to the attosecond timescale.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Loh, N. D. et al. Fractal morphology, imaging and mass spectrometry of single aerosol particles in flight. Nature 486, 513–517 (2012).
Barke, I. et al. The 3D-architecture of individual free silver nanoparticles captured by X-ray scattering. Nat. Commun. 6, 6187 (2015).
Gomez, L. F. et al. Shapes and vorticities of superfluid helium nanodroplets. Science 345, 906–909 (2014).
van der Schot, G. et al. Imaging single cells in a beam of live cyanobacteria with an X-ray laser. Nat. Commun. 6, 5704 (2015).
Seibert, M. M. et al. Single mimivirus particles intercepted and imaged with an X-ray laser. Nature 470, 78–81 (2011).
Neutze, R., Wouts, R., van der Spoel, D., Weckert, E. & Hajdu, J. Potential for biomolecular imaging with femtosecond X-ray pulses. Nature 406, 752–757 (2000).
Chapman, H. N. et al. Femtosecond X-ray protein nanocrystallography. Nature 470, 73–77 (2011).
Bostedt, C. et al. Ultrafast X-ray scattering of Xenon nanoparticles: imaging transient states of matter. Phys. Rev. Lett. 108, 093401 (2012).
Gorkhover, T. et al. Femtosecond and nanometre visualization of structural dynamics in superheated nanoparticles. Nat. Photon. 10, 93–97 (2016).
Miao, J, Sayre, D. & Chapman, H. Phase retrieval from the magnitude of the Fourier transforms of nonperiodic objects. J. Opt. Soc. Am A 15, 1662–1669 (1998).
Marchesini, S. et al. X-ray image reconstruction from a diffraction pattern alone. Phys. Rev. B 68, 140101(R) (2003).
Chapman, H. N. & Nugent, K. A. Coherent lensless X-ray imaging. Nat. Photon. 4, 833–839 (2010).
Gabor, D. et al. A new microscopic principle. Nature 161, 777–778 (1948).
Goodman, J. W. Introduction to Fourier Optics (Roberts and Company, Columbus, OH, USA, 2005).
Eisebitt, S. et al. Lensless imaging of magnetic nanostructures by X-ray. Nature 432, 885–888 (2004).
Schlotter, W. et al. Multiple reference Fourier transform holography with soft x rays. Appl. Phys. Lett. 89, 163112 (2006).
Marchesini, S. et al. Massively parallel X-ray holography. Nat. Photon. 2, 560–563 (2008).
Geilhufe, J. et al. Extracting depth information of 3-dimensional structures from a single-view X-ray Fourier-transform hologram. Opt. Express 22, 24959–24969 (2014).
Guehrs, E. et al. Wavefield back-propagation in high-resolution X-ray holography with a movable field of view. Opt. Express 18, 18922–18931 (2010).
Shintake, T. Possibility of single biomolecule imaging with coherent amplification of weak scattering X-ray photons. Phys. Rev. E 78, 041906 (2008).
Chamard, V. et al. Three-dimensional X-ray Fourier transform holography: the Bragg case. Phys. Rev. Lett. 104, 165501 (2010).
Xiao, C. et al. Structural studies of the giant Mimivirus. PLoS Biol. 7, 0958–0966 (2009).
Ferguson, K. R. et al. The atomic, molecular and optical science instrument at the linac coherent light source. J. Synchrot. Radiat. 22, 492–497 (2015).
Guinier, A. & Fournet, G. Small-Angle Scattering of X-Rays (Wiley, New York, USA, 1955).
Bostedt, C. et al. Clusters in intense FLASH pulses: ultrafast ionization dynamics and electron emission studied with spectroscopic and scattering techniques. J. Phys. B 12, 083004 (2010).
Schropp, A. & Schroer, C. G. Dose requirements for resolving a given feature in an object by coherent X-ray diffraction imaging. New. J. Phys. 12, 035016 (2010).
Hantke, M. et al. High-throughput imaging of heterogeneous cell organelles with an X-ray laser. Nat. Photon. 8, 943–949 (2014).
Rupp, D. et al. Coherent diffractive imaging of single helium nanodroplets with a high harmonic generation source. Nat. Commun. 8, 493 (2017).
Zherebtsov, S. et al. Controlled near-field enhanced electron acceleration from dielectric nanospheres with intense few-cycle laser fields. Nat. Phys. 7, 656–662 (2011).
Gorkhover, T. et al Nanoplasma dynamics of single large xenon clusters irradiated with superintense X-ray pulses from the Linac coherent light source free-electron laser. Phys. Rev. Lett 108, 245005 (2012).
Ekeberg, T. et al. Three-dimensional reconstruction of the giant Mimivirus particle with an X-ray free-electron laser. Phys. Rev. Lett. 114, 098102 (2015).
Emma, P. et al. First lasing and operation of an å ngstrom-wavelength free-electron laser. Nat. Photon. 4, 641–647 (2010).
Rupp, D. et al. Identification of twinned gas phase clusters by single-shot scattering with intense soft X-ray pulses. New. J. Phys. 14, 055016 (2012).
Rupp, D. et al. Generation and structure of extremely large clusters in pulsed jets. J. Chem. Phys. 141, 044306 (2014).
Gutt, C. et al. Single shot spatial and temporal coherence properties of the SLAC LINAC coherent light source in the hard X-ray regime. Phys. Rev. Lett. 108, 024801 (2012).
Andritschke, R., Hartner, G., Hartmann, R., Meidinger, N. & Struder, L. Data analysis for characterizing pnCCDs. In Nuclear Science Symposium Conference Record 2008 2166–2172 (IEEE, 2008).
Strüder, L. et al. Large-format, high-speed, X-ray pnCCDs combined with electron and ion imaging spectrometers in a multipurpose chamber for experiments at 4th generation light sources. Nucl. Instrum. Meth. A 614, 483–496 (2010).
Howells, M. et al. Toward a practical X-ray Fourier holography at high resolution. Nucl. Instrum. Meth. A 467, 864–867 (2001).
He, H. et al. Use of extended and prepared reference objects in experimental Fourier transform X-ray holography. Appl. Phys. Lett. 85, 2454–2456 (2004).
Acknowledgements
We would like to thank J. Geilhufe, E. Guehrs, A. Schropp and S. Eisebitt for many helpful discussions. T.G. acknowledges the P. Ewald fellowship from the Volkswagen Foundation and the Panofsky fellowship from SLAC National Accelerator Laboratory. We would like to thank J. Segal and A. Tomada from SLAC for providing high-resistivity Si wafers. Parts of this research were carried out at the Linac Coherent Light Source (LCLS) at the SLAC National Accelerator Laboratory. LCLS is an Office of Science User Facility operated for the US Department of Energy Office of Science by Stanford University. This work is supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences under contract no. DE-AC02-06CH11357 and contract no. DE-AC02-76SF00515. T.M. acknowledges financial support from BMBF (German Federal Ministry of Education and Research) projects 05K10KT2 and 05K13KT2 as well as DFG (German Research Foundation) BO3169/2-2. This work was supported by the Swedish Research Council, the Knut and Alice Wallenberg Foundation, the European Research Council, the Röntgen-Angström Cluster, ELI Extreme Light Infrastructure Phase 2 (CZ.02.1.01/0.0/0.0/15 008/0000162), ELIBIO (CZ.02.1.01/0.0/0.0/15 003/0000447) from the European Regional Development Fund, Material science and the Chalmers Area of Advance. F.R.N.C.M. acknowledges the Swedish Foundation for Strategic Research. Portions of this research were carried out at Brookhaven National Laboratory, operated under contract no. DE-SC0012704 from the US Department of Energy Office of Science. G.F. acknowledges the support of NKFIH K115504.
Author information
Authors and Affiliations
Contributions
T.G. conceived the concept of 'in-flight' holography with two sources with support from C.B., T.M. and J.H. The project was led by T.G., C.B., F.R.N.C.M. and J.H. The experimental setup was designed and the experiment was performed by all authors. The bioparticle injector was operated by J.B., M.Sei. and K.M.. The cluster source was operated by K.F., M.B., C.B. and T.G. The biological samples were prepared by D.H., D.S.D.L., K.O. and M.Sve. The online and offline data analysis was carried out by F.M., T.E., M.F.H., B.J.D., C.N., A.M., G.v.S., M.B. and K.F. The images were analysed and processed by A.U. and T.G. The results were interpreted by A.U. and T.G. with input from C.B., G.F., T.M., F.R.N.C.M. and J.H. The manuscript was written by T.G. and A.U. with contributions from C.B., G.F., T.M., F.M. and J.H. and input from all authors.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gorkhover, T., Ulmer, A., Ferguson, K. et al. Femtosecond X-ray Fourier holography imaging of free-flying nanoparticles. Nature Photon 12, 150–153 (2018). https://doi.org/10.1038/s41566-018-0110-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41566-018-0110-y
This article is cited by
-
3D atomic structure from a single X-ray free electron laser pulse
Nature Communications (2024)
-
Spatiotemporal observation of light propagation in a three-dimensional scattering medium
Scientific Reports (2021)
-
The role of transient resonances for ultra-fast imaging of single sucrose nanoclusters
Nature Communications (2020)
-
3D-printable portable open-source platform for low-cost lens-less holographic cellular imaging
Scientific Reports (2019)
-
Effect of ketyl radical on the structure and performance of holographic polymer/liquid-crystal composites
Science China Materials (2019)