Development of serial X-ray fluorescence holography for radiation-sensitive protein crystals
X-ray fluorescence holography (XFH) is a powerful atomic resolution technique capable of directly imaging the local atomic structure around atoms of a target element within a material. Although it is theoretically possible to use XFH to study the local structures of metal clusters in large protein c...
| Main Authors: | , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
International Union of Crystallography
2023-03-01
|
| Series: | Journal of Synchrotron Radiation |
| Subjects: | |
| Online Access: | http://scripts.iucr.org/cgi-bin/paper?S1600577522011833 |
| _version_ | 1811157603922739200 |
|---|---|
| author | Artoni Kevin R. Ang Yasufumi Umena Ayana Sato-Tomita Naoya Shibayama Naohisa Happo Riho Marumi Yuta Yamamoto Koji Kimura Naomi Kawamura Yu Takano Tomohiro Matsushita Yuji C. Sasaki Jian-Ren Shen Kouichi Hayashi |
| author_facet | Artoni Kevin R. Ang Yasufumi Umena Ayana Sato-Tomita Naoya Shibayama Naohisa Happo Riho Marumi Yuta Yamamoto Koji Kimura Naomi Kawamura Yu Takano Tomohiro Matsushita Yuji C. Sasaki Jian-Ren Shen Kouichi Hayashi |
| author_sort | Artoni Kevin R. Ang |
| collection | DOAJ |
| description | X-ray fluorescence holography (XFH) is a powerful atomic resolution technique capable of directly imaging the local atomic structure around atoms of a target element within a material. Although it is theoretically possible to use XFH to study the local structures of metal clusters in large protein crystals, the experiment has proven difficult to perform, especially on radiation-sensitive proteins. Here, the development of serial X-ray fluorescence holography to allow the direct recording of hologram patterns before the onset of radiation damage is reported. By combining a 2D hybrid detector and the serial data collection used in serial protein crystallography, the X-ray fluorescence hologram can be directly recorded in a fraction of the measurement time needed for conventional XFH measurements. This approach was demonstrated by obtaining the Mn Kα hologram pattern from the protein crystal Photosystem II without any X-ray-induced reduction of the Mn clusters. Furthermore, a method to interpret the fluorescence patterns as real-space projections of the atoms surrounding the Mn emitters has been developed, where the surrounding atoms produce large dark dips along the emitter–scatterer bond directions. This new technique paves the way for future experiments on protein crystals that aim to clarify the local atomic structures of their functional metal clusters, and for other related XFH experiments such as valence-selective XFH or time-resolved XFH. |
| first_indexed | 2024-04-10T05:10:03Z |
| format | Article |
| id | doaj.art-04c7cbec2a3d47d0a2d93dbfe96f4b5b |
| institution | Directory Open Access Journal |
| issn | 1600-5775 |
| language | English |
| last_indexed | 2024-04-10T05:10:03Z |
| publishDate | 2023-03-01 |
| publisher | International Union of Crystallography |
| record_format | Article |
| series | Journal of Synchrotron Radiation |
| spelling | doaj.art-04c7cbec2a3d47d0a2d93dbfe96f4b5b2023-03-09T09:18:19ZengInternational Union of CrystallographyJournal of Synchrotron Radiation1600-57752023-03-0130236837810.1107/S1600577522011833rv5166Development of serial X-ray fluorescence holography for radiation-sensitive protein crystalsArtoni Kevin R. Ang0Yasufumi Umena1Ayana Sato-Tomita2Naoya Shibayama3Naohisa Happo4Riho Marumi5Yuta Yamamoto6Koji Kimura7Naomi Kawamura8Yu Takano9Tomohiro Matsushita10Yuji C. Sasaki11Jian-Ren Shen12Kouichi Hayashi13Department of Physical Science and Engineering, Nagoya Institute of Technology, Gokiso, Showa, Nagoya 466-8555, JapanSynchrotron Radiation Research Center, Nagoya University, Furo, Chikusa, Nagoya 466-8603, JapanDivision of Biophysics, Department of Physiology, Jichi Medical University, Yakushiji, Shimotsuke, Tochigi 329-0498, JapanDivision of Biophysics, Department of Physiology, Jichi Medical University, Yakushiji, Shimotsuke, Tochigi 329-0498, JapanDepartment of Computer and Network Engineering, Graduate School of Information Sciences, Hiroshima City University, Asa-Minami-ku, Hiroshima 731-3194, JapanDepartment of Physical Science and Engineering, Nagoya Institute of Technology, Gokiso, Showa, Nagoya 466-8555, JapanDepartment of Physical Science and Engineering, Nagoya Institute of Technology, Gokiso, Showa, Nagoya 466-8555, JapanDepartment of Physical Science and Engineering, Nagoya Institute of Technology, Gokiso, Showa, Nagoya 466-8555, JapanJapan Synchrotron Radiation Research Institute (JASRI), Sayo, Hyôgo 679-5198, JapanGraduate School of Information Sciences, Hiroshima City University, Asa-Minami-ku, Hiroshima 731-3194, JapanGraduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma 630-0192, JapanGraduate School of Frontier Sciences, University of Tokyo, Kashiwa, Chiba 277-8561, JapanResearch Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University, Tsushima Naka, Okayama 700-8530, JapanDepartment of Physical Science and Engineering, Nagoya Institute of Technology, Gokiso, Showa, Nagoya 466-8555, JapanX-ray fluorescence holography (XFH) is a powerful atomic resolution technique capable of directly imaging the local atomic structure around atoms of a target element within a material. Although it is theoretically possible to use XFH to study the local structures of metal clusters in large protein crystals, the experiment has proven difficult to perform, especially on radiation-sensitive proteins. Here, the development of serial X-ray fluorescence holography to allow the direct recording of hologram patterns before the onset of radiation damage is reported. By combining a 2D hybrid detector and the serial data collection used in serial protein crystallography, the X-ray fluorescence hologram can be directly recorded in a fraction of the measurement time needed for conventional XFH measurements. This approach was demonstrated by obtaining the Mn Kα hologram pattern from the protein crystal Photosystem II without any X-ray-induced reduction of the Mn clusters. Furthermore, a method to interpret the fluorescence patterns as real-space projections of the atoms surrounding the Mn emitters has been developed, where the surrounding atoms produce large dark dips along the emitter–scatterer bond directions. This new technique paves the way for future experiments on protein crystals that aim to clarify the local atomic structures of their functional metal clusters, and for other related XFH experiments such as valence-selective XFH or time-resolved XFH.http://scripts.iucr.org/cgi-bin/paper?S1600577522011833x-ray fluorescence holographyatomic structuresprotein structures |
| spellingShingle | Artoni Kevin R. Ang Yasufumi Umena Ayana Sato-Tomita Naoya Shibayama Naohisa Happo Riho Marumi Yuta Yamamoto Koji Kimura Naomi Kawamura Yu Takano Tomohiro Matsushita Yuji C. Sasaki Jian-Ren Shen Kouichi Hayashi Development of serial X-ray fluorescence holography for radiation-sensitive protein crystals Journal of Synchrotron Radiation x-ray fluorescence holography atomic structures protein structures |
| title | Development of serial X-ray fluorescence holography for radiation-sensitive protein crystals |
| title_full | Development of serial X-ray fluorescence holography for radiation-sensitive protein crystals |
| title_fullStr | Development of serial X-ray fluorescence holography for radiation-sensitive protein crystals |
| title_full_unstemmed | Development of serial X-ray fluorescence holography for radiation-sensitive protein crystals |
| title_short | Development of serial X-ray fluorescence holography for radiation-sensitive protein crystals |
| title_sort | development of serial x ray fluorescence holography for radiation sensitive protein crystals |
| topic | x-ray fluorescence holography atomic structures protein structures |
| url | http://scripts.iucr.org/cgi-bin/paper?S1600577522011833 |
| work_keys_str_mv | AT artonikevinrang developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT yasufumiumena developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT ayanasatotomita developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT naoyashibayama developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT naohisahappo developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT rihomarumi developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT yutayamamoto developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT kojikimura developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT naomikawamura developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT yutakano developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT tomohiromatsushita developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT yujicsasaki developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT jianrenshen developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals AT kouichihayashi developmentofserialxrayfluorescenceholographyforradiationsensitiveproteincrystals |