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Single mimivirus particles intercepted and imaged with an X-ray laser

Nature volume 470, pages 7881 (03 February 2011) | Download Citation

Abstract

X-ray lasers offer new capabilities in understanding the structure of biological systems, complex materials and matter under extreme conditions1,2,3,4. Very short and extremely bright, coherent X-ray pulses can be used to outrun key damage processes and obtain a single diffraction pattern from a large macromolecule, a virus or a cell before the sample explodes and turns into plasma1. The continuous diffraction pattern of non-crystalline objects permits oversampling and direct phase retrieval2. Here we show that high-quality diffraction data can be obtained with a single X-ray pulse from a non-crystalline biological sample, a single mimivirus particle, which was injected into the pulsed beam of a hard-X-ray free-electron laser, the Linac Coherent Light Source5. Calculations indicate that the energy deposited into the virus by the pulse heated the particle to over 100,000 K after the pulse had left the sample. The reconstructed exit wavefront (image) yielded 32-nm full-period resolution in a single exposure and showed no measurable damage. The reconstruction indicates inhomogeneous arrangement of dense material inside the virion. We expect that significantly higher resolutions will be achieved in such experiments with shorter and brighter photon pulses focused to a smaller area. The resolution in such experiments can be further extended for samples available in multiple identical copies.

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Acknowledgements

This work was supported by the following agencies: the Swedish Research Councils; the Swedish Foundation for International Cooperation in Research and Higher Education; Stiftelsen Olle Engkvist Byggmästare; the Swedish University of Agricultural Sciences; the Helmholtz Association (VH-VI-302); the DFG Cluster of Excellence at the Munich Centre for Advanced Photonics; the Centre National de la Recherche Scientifique; Agence Nationale de la Recherche (ANR-BLAN08-0089); the Hamburg Ministry of Science and Research and Joachim Herz Stiftung, as part of the Hamburg Initiative for Excellence in Research (LEXI); the Hamburg School for Structure and Dynamics; the Max Planck Society, the US National Science Foundation (grants MCB 0919195 and MCB-1021557); and the US Department of Energy, through the PULSE Institute. Portions of this research were carried out at the Linac Coherent Light Source, a National User Facility operated by Stanford University on behalf of the US Department of Energy, Office of Basic Energy Sciences. We are grateful to B. Hedman and N. Timneanu for their help and to the scientific and technical staff of the LCLS for their outstanding facility and support.

Author information

Author notes

    • M. Marvin Seibert
    • , Tomas Ekeberg
    •  & Filipe R. N. C. Maia

    These authors contributed equally to this work.

Affiliations

  1. Laboratory of Molecular Biophysics, Department of Cell and Molecular Biology, Uppsala University, Husargatan 3 (Box 596), SE-751 24 Uppsala, Sweden

    • M. Marvin Seibert
    • , Tomas Ekeberg
    • , Filipe R. N. C. Maia
    • , Martin Svenda
    • , Jakob Andreasson
    • , Olof Jönsson
    • , Duško Odić
    • , Bianca Iwan
    • , Andrea Rocker
    • , Daniel Westphal
    • , Max Hantke
    • , Carl Caleman
    •  & Janos Hajdu
  2. Center for Free-Electron Laser Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany

    • Daniel P. DePonte
    • , Anton Barty
    • , Joachim Schulz
    • , Lars Gumprecht
    • , Nicola Coppola
    • , Andrew Aquila
    • , Mengning Liang
    • , Thomas A. White
    • , Andrew Martin
    • , Carl Caleman
    • , Stephan Stern
    •  & Henry N. Chapman
  3. University of Hamburg, Notkestrasse 85, 22607 Hamburg, Germany

    • Stephan Stern
    •  & Henry N. Chapman
  4. Information Génomique et Structurale, CNRS-UPR2589, Aix-Marseille Université, Institut de Microbiologie de la Méditerranée, Parc Scientifique de Luminy, Case 934, 13288 Marseille Cedex 9, France

    • Chantal Abergel
    • , Virginie Seltzer
    •  & Jean-Michel Claverie
  5. LCLS, SLAC National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, California 94025, USA

    • Christoph Bostedt
    • , John D. Bozek
    • , Sébastien Boutet
    • , A. Alan Miahnahri
    • , Marc Messerschmidt
    • , Jacek Krzywinski
    •  & Garth Williams
  6. PULSE Institute, SLAC National Accelerator Laboratory, 2575 Sand Hill Road, Menlo Park, California 94025, USA

    • Keith O. Hodgson
    • , Michael J. Bogan
    • , Christina Y. Hampton
    • , Raymond G. Sierra
    •  & Dmitri Starodub
  7. Department of Molecular Biology, Swedish University of Agricultural Sciences, Uppsala Biomedical Centre, Box 590, S-751 24 Uppsala, Sweden

    • Inger Andersson
  8. Photon Science, DESY, Notkestrasse 85, 22607 Hamburg, Germany

    • Saša Bajt
    • , Miriam Barthelmess
    • , Helmut Hirsemann
    • , Guillaume Potdevin
    • , Heinz Graafsma
    •  & Björn Nilsson
  9. Department of Physics, PSF470, Arizona State University, Tempe, Arizona 85287-1504, USA

    • John C. H. Spence
    • , Uwe Weierstall
    • , Richard Kirian
    •  & R. Bruce Doak
  10. Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA

    • Petra Fromme
    •  & Mark Hunter
  11. Advanced Light Source, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA

    • Stefano Marchesini
  12. Lawrence Livermore National Laboratory, 7000 East Avenue, Mail Stop L-211, Livermore, California 94551, USA

    • Stefan P. Hau-Riege
    •  & Matthias Frank
  13. Max-Planck-Institut für Medizinische Forschung, Jahnstrasse 29, 69120 Heidelberg, Germany

    • Robert L. Shoeman
    • , Lukas Lomb
    • , Daniel Rolles
    • , Lutz Foucar
    • , Ilme Schlichting
    • , Faton Krasniqi
    •  & Mario Bott
  14. Max Planck Advanced Study Group, Center for Free-Electron Laser Science, Notkestrasse 85, 22607 Hamburg, Germany

    • Sascha W. Epp
    • , Daniel Rolles
    • , Artem Rudenko
    • , Carlo Schmidt
    • , Lutz Foucar
    • , Benedikt Rudek
    • , Benjamin Erk
    • , André Hömke
    • , Lothar Strüder
    • , Joachim Ullrich
    • , Ilme Schlichting
    •  & Faton Krasniqi
  15. Max-Planck-Institut für Kernphysik, Saupfercheckweg 1, 69117 Heidelberg, Germany

    • Sascha W. Epp
    • , Artem Rudenko
    • , Carlo Schmidt
    • , Benedikt Rudek
    • , Benjamin Erk
    • , André Hömke
    • , Joachim Ullrich
    • , Kai-Uwe Kühnel
    •  & Claus-Dieter Schröter
  16. PNSensor GmbH, Römerstrasse 28, 80803 München, Germany

    • Robert Hartmann
    • , Peter Holl
    • , Christian Reich
    •  & Heike Soltau
  17. Max-Planck-Institut Halbleiterlabor, Otto-Hahn-Ring 6, 81739 München, Germany

    • Nils Kimmel
    • , Daniel Pietschner
    • , Georg Weidenspointner
    • , Lothar Strüder
    • , Günter Hauser
    • , Sven Herrmann
    • , Gerhard Schaller
    • , Florian Schopper
    •  & Robert Andritschke
  18. Max-Planck-Institut für Extraterrestrische Physik, Giessenbachstrasse, 85741 Garching, Germany

    • Nils Kimmel
    • , Daniel Pietschner
    • , Georg Weidenspointner
    • , Lothar Strüder
    • , Günter Hauser
    • , Sven Herrmann
    • , Gerhard Schaller
    • , Florian Schopper
    •  & Robert Andritschke
  19. Universität Siegen, Emmy-Noether Campus, Walter Flex Strasse 3, 57068 Siegen, Germany

    • Lothar Strüder
  20. Forschungszentrum Jülich, Institut ZEL, 52425 Jülich, Germany

    • Hubert Gorke
  21. Institut für Optik und Atomare Physik, Technische Universität Berlin, Hardenbergstrasse 36, 10623 Berlin, Germany

    • Sebastian Schorb
    • , Daniela Rupp
    • , Marcus Adolph
    •  & Tais Gorkhover

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Contributions

J.H. and H.N.C. conceived the experiment. C.A., V.S., J.-M.C., M.S., O.J., A. Rocker, I.A. and D.O. prepared and characterized the samples. J.D.B., C.B. and K.O.H. created the LCLS beamline. J.H., H.N.C., J.S., L.G., A.B., N.C., A.A., A.M., J.K., K.O.H. and S.P.H.-R. developed the imaging concept. S.W.E., R.H., D. Rolles, A. Rudenko, C.S., L.F., N.K., P.H., B.R., B.E., A.H., Ch.R., D.P., G.W., L.S., G.H., H. Gorke, J.U., I.S., S.H., G.S., F.S., H.S., K.-U.K., R.A., C.-D.S., F.K., M. Bott, S. Schorb, D. Rupp, M.A., T.G., H.H., L.G., G.P., H. Graafsma and B.N. designed and set up the CAMP instrument and/or developed and operated the pnCCD detectors. S. Bajt and M. Barthelmess coordinated instrumentation, worked on engineering and prepared filters and calibration samples. J.K., S.P.H.-R., A.B., H.N.C., J.S., A.M. and N.C. characterized the focus. B.I., D.W., M.S., M.M.S. and J.H. built the sample injector. D.P.D., J.H., M.S., D.W., U.W., R.K., M. Hunter, R.B.D. and J.C.H.S. designed and built the nanospray nebulizer. J.H., M.S., M.M.S., F.R.N.C.M., J.A., A.A.M., A. Rocker, M.J.B., C.Y.H., R.G.S., S. Boutet, I.A., O.J., D.S., A.B., J.S., D.P.D., A.A., M.L., J.K., T.A.W., A.M., R.L.S., L.L., M. Barthelmess, J.C.H.S., P.F., I.S., U.W., R.K., M. Hunter, R.B.D., M.F., G.W., M. Bott, S.W.E., B.E., L.F., R.H., N.K., L.L., D. Rupp, B.R., A. Rudenko, R.L.S., L.S., I.S., C.S., J.U. and H.N.C. characterized the imaging apparatus and carried out the experiment. T.E., F.R.N.C.M., M. Hantke, M.M.S., A.B., T.A.W., A.M., A.A., S.M., M.M. and J.H. analysed the data. T.E., F.R.N.C.M., A.B. and S.M. performed image reconstructions. J.H. and T.E. wrote the manuscript with input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Chantal Abergel or Janos Hajdu.

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https://doi.org/10.1038/nature09748

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