X-Ray Spectroscopy with XFELs

  • Roberto Alonso-Mori
  • Junko Yano


The use of XFELs in the last 10 years has produced multiple opportunities to undertake scientific questions that could not be addressed using other types of X-ray sources, in particular for femtosecond and picosecond processes and for radiation sensitive and scarce biological samples. X-ray spectroscopy, the experimental approach used in many of these studies, is well established and has been broadly used at synchrotron radiation sources worldwide for the last few decades. However to take advantage of spectroscopic tools at XFELs, synchrotron-based methods have to be adapted to the unique characteristics of the XFEL beam, like its pulsed nature and time structure, as well as the effects induced in the sample derived from these properties. In the few short years of XFEL operations, various studies relied on spectroscopic methods, both in the hard and in the soft X-ray regime. In this chapter, we will provide an inclusive review of recent XFEL spectroscopic studies on biological samples and focus on the description of the experimental aspects of such measurements. We will include a discussion on spectroscopy technique developments that are unique to XFELs with the potential to make an impact on the field.



R. A.-M. and J.Y. acknowledge all the collaborators of the research presented in this chapter. Use of the Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory, is supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences under Contract No. DE-AC02-76SF00515. J.Y. thanks the Director, Office of Science, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences of the Department of Energy under contract DE-AC02-05CH11231, and the NIH Grants GM110501 and GM055302, which contribute to supporting some of the research presented in this chapter.


  1. 1.
    Yano, J., Kern, J., Irrgang, K. D., Latimer, M. J., Bergmann, U., Glatzel, P., et al. (2005). Proceedings of the National Academy of Sciences of the United States of America, 102(34), 12047–12052.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Garman, E., & Weik, M. (2017). Journal of Synchrotron Radiation, 24(1), 1–6.PubMedCrossRefGoogle Scholar
  3. 3.
    Holton, J. (2009). Journal of Synchrotron Radiation, 16(2), 133–142.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Lemke, H., Weaver, M., Chollet, M., Robinson, J., Glownia, J. M., Bionta, M. R., et al. (2013). Proceedings of SPIE, 8778, 87780S.CrossRefGoogle Scholar
  5. 5.
    Margaritondo, G., & Ribic, P. R. (2011). Journal of Synchrotron Radiation, 18, 101–108.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Emma, P., Akre, R., Arthur, J., Bionta, R., Bostedt, C., Bozek, J., et al. (2010). Nature Photonics, 4, 641–647.CrossRefGoogle Scholar
  7. 7.
    Ishikawa, T., Aoyagi, H., Asaka, T., Asano, Y., Azumi, N., Bizen, T., et al. (2012). Nature Photonics, 6, 540–544.CrossRefGoogle Scholar
  8. 8.
    Chapman, H. N., Fromme, P., Barty, A., White, T., Kirian, R., Aquila, A., et al. (2011). Nature, 470(7332), 73–77.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Nass, K., Foucar, L., Barends, T. R. M., Hartmann, E., Botha, S., Shoeman, R. L., et al. (2015). Journal of Synchrotron Radiation, 22(2), 225–238.PubMedCrossRefGoogle Scholar
  10. 10.
    Boutet, S., Lomb, L., Williams, G. J., Barends, T. R. M., Aquila, A., Doak, R. B., et al. (2012). Science, 337, 362–364.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Alonso-Mori, R., Kern, J., Gildea, R. J., Sokaras, D., Weng, T.-C., Lassalle-Kaiser, B., et al. (2012). Proceedings of the National Academy of Sciences of the United States of America, 109(47), 19103–19107.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Weierstall, U. (2014). Philosophical Transactions of the Royal Society B, 369, 20130337.CrossRefGoogle Scholar
  13. 13.
    Weierstall, U., Doak, R. B., Spence, J. C. H., Starodub, D., Shapiro, D., Kennedy, P., et al. (2008). Experiments in Fluids, 44, 675.CrossRefGoogle Scholar
  14. 14.
    Roessler, C. G., Kuczewski, A., Stearns, R., Ellson, R., Olechno, J., Orville, A. M., et al. (2013). Journal of Synchrotron Radiation, 20, 805–808.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Roessler, C. G., Agarwal, R., Allaire, M., Alonso-Mori, R., Andi, B., Bachega, J. F. R., et al. (2016). Structure, 24(4), 631–640.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Fuller, F. D., Gul, S., Chatterjee, R., Burgie, E. S., Young, I. D., Lebrette, H., et al. (2017). Nature Methods, 14(4), 443–449.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Milathianaki, D., Boutet, S., Williams, G. J., Higginbotham, A., Ratner, D., Gleason, A. E., et al. (2013). Science, 342(6155), 220–223.PubMedCrossRefGoogle Scholar
  18. 18.
    Wittenberg, J. S., Miller, T. A., Szilagyi, E., Lutker, K., Quirin, F., Lu, W., et al. (2014). Nano Letters, 14(4), 1995–1999.PubMedCrossRefGoogle Scholar
  19. 19.
    Roedig, P., Ginn, H. M., Pakendorf, T., Sutton, G., Harlos, K., Walter, T. S., et al. (2017). Nature Methods, 14, 805–810.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Koningsberger, D., & Prins, R. (1988). X-Ray absorption: Principles, applications, techniques of EXAFS, SEXAFS and XANES. New York: Wiley.Google Scholar
  21. 21.
    Amann, J., Berg, W., Blank, V., Decker, F. J., Ding, Y., Emma, P., et al. (2012). Nature Photonics, 6, 693.CrossRefGoogle Scholar
  22. 22.
    Kroll, T., Kern, J., Kubin, M., Ratner, D., Gul, S., Fuller, F. D., et al. (2016). Optics Express, 24(20), 22469–22480.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Lemke, H. T., Bressler, C., Chen, L. X., Fritz, D. M., Gaffney, K. J., Galler, A., et al. (2013). The Journal of Physical Chemistry A, 117, 735–740.PubMedCrossRefGoogle Scholar
  24. 24.
    Cammarata, M., Bertoni, R., Lorenc, M., Cailleau, H., Di Matteo, S., Mauriac, C., et al. (2014). Physical Review Letters, 113, 227402.PubMedCrossRefGoogle Scholar
  25. 25.
    Levantino, M., Lemke, H. T., Schirò, G., Glownia, M., Cupane, A., Cammarata, M., et al. (2015). Structural Dynamics, 2(4), 041713.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Shelby, M. L., Lestrange, P. J., Jackson, N. E., Haldrup, K., Mara, M. W., Stickrath, A. B., et al. (2016). Journal of the American Chemical Society, 138, 8752–8764.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Marino, A., Cammarata, M., Matar, S. F., Ltard, J.-F., Chastanet, G., Chollet, M., et al. (2016). Structural Dynamics, 3(2), 023605.PubMedCrossRefGoogle Scholar
  28. 28.
    Miller, N. A., Deb, A., Alonso-Mori, R., Garabato, B. D., Glownia, J. M., Kiefer, L., et al. (2017). Journal of the American Chemical Society, 139(5), 1894–1899.PubMedCrossRefGoogle Scholar
  29. 29.
    Zhu, D., Cammarata, M., Feldkamp, J., Fritz, D., Hastings, J., Lee, S., et al. (2013). Journal of Physics Conference Series, 425, 052033.CrossRefGoogle Scholar
  30. 30.
    Obara, Y., Katayama, T., Ogi, Y., Suzuki, T., Kurahashi, N., Karashima, S., et al. (2013). Optics Express, 22(1), 1105–1113.CrossRefGoogle Scholar
  31. 31.
    Katayama, T., Inubushi, Y., Obara, Y., Sato, T., Togashi, T., Tono, K., et al. (2013). Applied Physics Letters, 103, 131105.CrossRefGoogle Scholar
  32. 32.
    Ogi, Y., Obara, Y., Katayama, T., Suzuki, Y.-I., Liu, S. Y., Bartlett, N. C.-M., et al. (2015). Structural Dynamics, 2, 034901.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Gaudin, J., Fourment, C., Cho, B. I., Engelhorn, K., Galtier, E., Harmand, M., et al. (2014). Scientific Reports, 4, 4724.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Stöhr, J. (1992). NEXAFS spectroscopy. Berlin: Springer.CrossRefGoogle Scholar
  35. 35.
    Friedrich, S., Funk, T., Drury, O., Labov, S., & Cramer, S. (2002). Review of Scientific Instruments, 73(3), 1629.CrossRefGoogle Scholar
  36. 36.
    Mitzner, R., Rehanek, J., Kern, J., Gul, S., Hattne, J., Taguchi, T., et al. (2013). Journal of Physical Chemistry Letters, 4, 3641.PubMedCrossRefGoogle Scholar
  37. 37.
    Kubin, M., Kern, J., Gul, S., Kroll, T., Chatterjee, R., Löchel, H., et al. (2017). Structural Dynamics, 4, 054307.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Schreck, S., Beye, M., Sellberg, J. A., McQueen, T., Laksmono, H., Kennedy, B., et al. (2014). Physical Review Letters, 113, 153002.PubMedCrossRefGoogle Scholar
  39. 39.
    Glatzel, P., & Bergmann, U. (2005). Coordination Chemistry Reviews, 249(7), 65.CrossRefGoogle Scholar
  40. 40.
    Hamos, L. V. (1932). Naturwiss, 20, 705–706.CrossRefGoogle Scholar
  41. 41.
    Alonso-Mori, R., Kern, J., Sokaras, D., Weng, T.-C., Nordlund, D., Tran, R., et al. (2012). Review of Scientific Instruments, 83, 073114.PubMedCrossRefGoogle Scholar
  42. 42.
    Zhang, W., Alonso-Mori, R., Bergmann, U., Bressler, C., Chollet, M., Galler, A., et al. (2014). Nature, 509, 345–348.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Zhang, W., Kjr, K. S., Alonso-Mori, R., Bergmann, U., Chollet, M., Fredin, L. A., et al. (2017). Chemical Science, 8, 515–523.PubMedCrossRefGoogle Scholar
  44. 44.
    Canton, S. E., Kjr, K. S., Vank, G., van Driel, T. B., ichi Adachi, S., Bordage, A., et al. (2015). Nature Communications, 6, 6359.Google Scholar
  45. 45.
    Haldrup, K., Gawelda, W., Abela, R., Alonso-Mori, R., Bergmann, U., Bordage, A., et al. (2016). The Journal of Physical Chemistry B, 120, 1158–1168.PubMedCrossRefGoogle Scholar
  46. 46.
    Alonso-Mori, R., Asa, K., Bergmann, U., Brewster, A. S., Chatterjee, R., Cooper, J. K., et al. (2016). Faraday Discussions, 194, 621–638.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Kjr, K. S., Zhang, W., Alonso-Mori, R., Bergmann, U., Chollet, M., Hadt, R. G., et al. (2017). Structural Dynamics, 4(4), 044030.CrossRefGoogle Scholar
  48. 48.
    Kern, J., Alonso-Mori, R., Tran, R., Hattne, J., Gildea, R. J., Echols, N., et al. (2013). Science, 340(6131), 491–495.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Kern, J., Tran, R., Alonso-Mori, R., Koroidov, S., Echols, N., Hattne, J., et al. (2014). Nature Communications, 5, 4371.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Mara, M. W., Hadt, R. G., Reinhard, M. E., Kroll, T., Lim, H., Hartsock, R., et al. (2017). Science, 356(6344), 1276–1280.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Stojanoff, V., Hamalainen, K., Siddons, D. P., Hastings, J. B., Berman, I. E., Cramer, S., et al. (1992). Review of Scientific Instruments, 63(1), 1125–1127.CrossRefGoogle Scholar
  52. 52.
    Alonso-Mori, R., Sokaras, D., Zhu, D., Kroll, T., Chollet, M., Feng, Y., et al. (2015). Journal of Synchrotron Radiation, 22(3), 612–620.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Mori, R. A., Paris, E., Giuli, G., Eeckhout, S. G., Kavcic, M., Zitnik, M., et al. (2009). Analytical Chemistry, 81(15), 6516–6525.CrossRefGoogle Scholar
  54. 54.
    Mori, R. A., Paris, E., Giuli, G., Eeckhout, S. G., Kavc, M., Zitnik, M., et al. (2010). Inorganic Chemistry, 49(14), 6468–6473.PubMedCrossRefGoogle Scholar
  55. 55.
    Thomas, R., Kas, J., Glatzel, P., Samarai, M. A., de Groot, F. M., Mori, R. A., et al. (2015). Journal of Physical Chemistry C, 119(5), 2419–2426.Google Scholar
  56. 56.
    Beye, M., Anniyev, T., Coffee, R., DellAngela, M., Föhlisch, A., Gladh, J., et al. (2013). Physical Review Letters, 110, 186101.PubMedCrossRefGoogle Scholar
  57. 57.
    Nilsson, A., LaRue, J., Öberg, H., Ogasawara, H., Dell’Angela, M., Beye, M., et al. (2017). Chemical Physics Letters, 675, 145–173.CrossRefGoogle Scholar
  58. 58.
    Dell’Angela, M., Anniyev, T., Beye, M., Coffee, R., Föhlisch, A. Gladh, J., et al. (2013). Science, 339(6125), 1302–1305.PubMedCrossRefGoogle Scholar
  59. 59.
    Shavorskiy, A., Cordones, A., Vura-Weis, J., Siefermann, K., Slaughter, D., Sturm, F., et al. (2013). AIP Conference Proceedings, 1525, 475.CrossRefGoogle Scholar
  60. 60.
    Kroll, T., Weninger, C., Alonso-Mori, R., Sokaras, D., Zhu, D., Mercadier, L., et al. (2017). Physical review letters, 120(13), 133203.Google Scholar
  61. 61.
    Rohringer, N., Ryan, D., London, R. A., Purvis, M., Albert, F., Dunn, J., et al. (2012). English. Nature, 481(7382), 488–491.PubMedCrossRefGoogle Scholar
  62. 62.
    Kotani, A., & Shin, S. (2001). Reviews of Modern Physics, 73, 203.CrossRefGoogle Scholar
  63. 63.
    Kroll, T., Hadt, R. G., Wilson, S. A., Lundberg, M., Yan, J. J., Weng, T.-C., et al. (2014). Journal of the American Chemical Society, 136(52), 18087–18099.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Glatzel, P., Schroeder, H., Pushkar, Y., BoronIII, T., Mukherjee, S. G., Christo, V. L., et al. (2013). Inorganic Chemistry, 52(10), 5642–5644.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Franz, M. O., & Schölkopf, B. (2006). Neural Computation, 18(12), 3097–3118.PubMedCrossRefGoogle Scholar
  66. 66.
    Titus, C. J., Baker, M. L., Lee, S. J., mei Cho, H., Doriese, W. B., Fowler, J. W., et al. (2017). arXiv 1706.09878.Google Scholar
  67. 67.
    Wernet, P., Kunnus, K., Josefsson, I., Rajkovic, I., Quevedo, W., Beye, M., et al. (2015). Nature, 520, 78–81.CrossRefGoogle Scholar
  68. 68.
    Kunnus, K., Josefsson, I., Rajkovic, I., Schreck, S., Quevedo, W., Beye, M., et al. (2016). Structural Dynamics, 3(4), 043204.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Eckert, S., Norell, J., Miedema, P.S., Beye, M., Fondell, M., Quevedo, W., et al. (2017). Angewandte Chemie, International Edition, 56, 6088.CrossRefGoogle Scholar
  70. 70.
    Zhong, Y., Rehanek, J., Löchel, H., Braig, C., Buck, J., Firsov, A., et al. (2017). Optics Express, 25(10), 10984–10996.CrossRefGoogle Scholar
  71. 71.
    Qiao, R., Li, Q., Zhuo, Z., Sallis, S., Fuchs, O., Blum, M., et al. (2017). Review of Scientific Instruments, 88(3), 033106.PubMedCrossRefGoogle Scholar
  72. 72.
    Umena Y., Kawakami, K., Shen, J.-R., & Kamiya, N. (2011). Nature, 473, 55–60.CrossRefGoogle Scholar
  73. 73.
    Chollet, M., Alonso-Mori, R., Cammarata, M., Damiani, D., Defever, J., Delor, J. T., et al. (2015). Journal of Synchrotron Radiation, 22(3), 503–507.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Linac Coherent Light SourceSLAC National Accelerator LaboratoryMenlo ParkUSA
  2. 2.Molecular Biophysics and Integrated Bioimaging DivisionLawrence Berkeley National LaboratoryBerkeleyUSA

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