Title: Effects of x-ray free-electron laser pulse intensity on the Mn Kβ_1,3 x-ray emission spectrum in photosystem II—A case study for metalloprotein crystals and solutions

Abstract

In the last ten years, x-ray free-electron lasers (XFELs) have been successfully employed to characterize metalloproteins at room temperature using various techniques including x-ray diffraction, scattering, and spectroscopy. The approach has been to outrun the radiation damage by using femtosecond (fs) x-ray pulses. An example of an important and damage sensitive active metal center is the Mn₄CaO₅ cluster in photosystem II (PS II), the catalytic site of photosynthetic water oxidation. The combination of serial femtosecond x-ray crystallography and Kβ x-ray emission spectroscopy (XES) has proven to be a powerful multimodal approach for simultaneously probing the overall protein structure and the electronic state of the Mn₄CaO₅ cluster throughout the catalytic (Kok) cycle. As the observed spectral changes in the Mn₄CaO₅ cluster are very subtle, it is critical to consider the potential effects of the intense XFEL pulses on the Kβ XES signal. We report here a systematic study of the effects of XFEL peak power, beam focus, and dose on the Mn Kβ_1,3 XES spectra in PS II over a wide range of pulse parameters collected over seven different experimental runs using both microcrystal and solution PS II samples. Our findings show that for beam intensities ranging from ~5 x 10^15more » to 5 x 10¹⁷ W/cm² at a pulse length of ~35 fs, the spectral effects are small compared to those observed between S-states in the Kok cycle. Our results provide a benchmark for other XFEL-based XES studies on metalloproteins, confirming the viability of this approach.« less

Authors:

Fransson, Thomas  ^[1];

• Search DOE PAGES for author "Fransson, Thomas"
• Search DOE PAGES for ORCID "0000-0002-3770-9780"

Alonso-Mori, Roberto  ^[2];

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• Search DOE PAGES for ORCID "0000-0002-5357-0934"

Chatterjee, Ruchira  ^[3];

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• Search DOE PAGES for ORCID "0000-0002-0865-061X"

Cheah, Mun Hon  ^[4];

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• Search DOE PAGES for ORCID "0000-0001-5732-1524"

Ibrahim, Mohamed  ^[5];

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• Search DOE PAGES for ORCID "0000-0002-1431-9755"

Hussein, Rana  ^[5];

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• Search DOE PAGES for ORCID "0000-0001-6292-2375"

Zhang, Miao  ^[5];

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• Search DOE PAGES for ORCID "0000-0003-4022-7093"

Fuller, Franklin  ^[2];

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• Search DOE PAGES for ORCID "0000-0002-3773-7087"

Gul, Sheraz  ^[3];

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• Search DOE PAGES for ORCID "0000-0001-8920-8737"

Kim, In-Sik  ^[3];

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• Search DOE PAGES for ORCID "0000-0002-0258-6012"

Simon, Philipp S.  ^[3];

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• Search DOE PAGES for ORCID "0000-0002-2859-4475"

Bogacz, Isabel  ^[3];

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• Search DOE PAGES for ORCID "0000-0003-1493-3867"

Makita, Hiroki  ^[3];

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de Lichtenberg, Casper  ^[6];

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• Search DOE PAGES for ORCID "0000-0003-2975-8395"

Song, Sanghoon  ^[2];

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• Search DOE PAGES for ORCID "0000-0003-3493-1850"

Batyuk, Alexander  ^[2];

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• Search DOE PAGES for ORCID "0000-0002-9393-2880"

Sokaras, Dimosthenis  ^[7];

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Massad, Ramzi  ^[3];

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Doyle, Margaret  ^[3];

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Britz, Alexander  ^[2]

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more »; Weninger, Clemens  ^[8];

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• Search DOE PAGES for ORCID "0000-0002-7453-7914"

Zouni, Athina  ^[5];

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• Search DOE PAGES for ORCID "0000-0003-0561-6990"

Messinger, Johannes  ^[9];

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• Search DOE PAGES for ORCID "0000-0003-2790-7721"

Yachandra, Vittal K.  ^[3];

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• Search DOE PAGES for ORCID "0000-0002-3983-7858"

Yano, Junko  ^[3];

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• Search DOE PAGES for ORCID "0000-0001-6308-9071"

Kern, Jan F.  ^[3];

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• Search DOE PAGES for ORCID "0000-0002-7272-1603"

Bergmann, Uwe  ^[10]

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• Search DOE PAGES for ORCID "0000-0001-5639-166X"

« less

---

+ Show Author Affiliations

1. KTH Royal Inst. of Technology, Stockholm (Sweden)
2. SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
4. Uppsala Univ. (Sweden)
5. Humboldt Univ. of Berlin (Germany)
6. Uppsala Univ. (Sweden); Umea Univ. (Sweden); Univ. of Copenhagen (Denmark)
7. SLAC National Accelerator Lab., Menlo Park, CA (United States)
8. Lund Univ. (Sweden)
9. Uppsala Univ. (Sweden); Umea Univ. (Sweden)
10. Univ. of Wisconsin, Madison, WI (United States)

Publication Date:

Mon Nov 22 00:00:00 EST 2021

Research Org.:

SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Institutes of Health (NIH); US Air Force Office of Scientific Research (AFOSR); German Research Foundation (DFG); USDOE

OSTI Identifier:

1868899

Alternate Identifier(s):

OSTI ID: 1832063

Grant/Contract Number:  

AC02-76SF00515; GM055302: GM110501; GM126289; 1P41GM139687; GM117126; GM133081; GM124149; GM124169; 2016-05183; 2020-03809; 2017-00356; FA8655-20-1-2010; EXC2008/1-390540038; SfB1078; AC02-05CH11231; OBES

Resource Type:

Accepted Manuscript

Journal Name:

Structural Dynamics

Additional Journal Information:

Journal Volume: 8; Journal Issue: 6; Journal ID: ISSN 2329-7778

Publisher:

American Crystallographic Association/AIP

Country of Publication:

United States

Language:

English

Subject:

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES