Capturing structural changes of the S1to S2transition of photosystem II using time-resolved serial femtosecond crystallography

Hongjie Li, Yoshiki Nakajima, Takashi Nomura, Michihiro Sugahara, Shinichiro Yonekura, Siu Kit Chan, Takanori Nakane, Takahiro Yamane, Yasufumi Umena, Mamoru Suzuki, Tetsuya Masuda, Taiki Motomura, Hisashi Naitow, Yoshinori Matsuura, Tetsunari Kimura, Kensuke Tono, Shigeki Owada, Yasumasa Joti, Rie Tanaka, Eriko NangoFusamichi Akita, Minoru Kubo, So Iwata, Jian Ren Shen, Michihiro Suga

Research output: Contribution to journalArticlepeer-review

Abstract

Photosystem II (PSII) catalyzes light-induced water oxidation through an S i-state cycle, leading to the generation of di-oxygen, protons and electrons. Pump-probe time-resolved serial femtosecond crystallography (TR-SFX) has been used to capture structural dynamics of light-sensitive proteins. In this approach, it is crucial to avoid light contamination in the samples when analyzing a particular reaction intermediate. Here, a method for determining a condition that avoids light contamination of the PSII microcrystals while minimizing sample consumption in TR-SFX is described. By swapping the pump and probe pulses with a very short delay between them, the structural changes that occur during the S1-to-S2 transition were examined and a boundary of the excitation region was accurately determined. With the sample flow rate and concomitant illumination conditions determined, the S2-state structure of PSII could be analyzed at room temperature, revealing the structural changes that occur during the S1-to-S2 transition at ambient temperature. Though the structure of the manganese cluster was similar to previous studies, the behaviors of the water molecules in the two channels (O1 and O4 channels) were found to be different. By comparing with the previous studies performed at low temperature or with a different delay time, the possible channels for water inlet and structural changes important for the water-splitting reaction were revealed.

Original languageEnglish
Pages (from-to)431-443
Number of pages13
JournalIUCrJ
Volume8
DOIs
Publication statusPublished - May 1 2021
Externally publishedYes

Keywords

  • X-ray free-electron lasers
  • membrane proteins
  • molecular movies
  • photosystem II
  • protein structures
  • serial crystallography
  • time-resolved serial crystallography

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry
  • Materials Science(all)
  • Condensed Matter Physics

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