Capturing structural changes of the S1 to S2 transition of photosystem II using time-resolved serial femtosecond crystallography

IUCrJ. 2021 Apr 7;8(Pt 3):431-443. doi: 10.1107/S2052252521002177. eCollection 2021 May 1.

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.

Keywords: X-ray free-electron lasers; membrane proteins; molecular movies; photosystem II; protein structures; serial crystallography; time-resolved serial crystallography.

Grants and funding

This work was funded by Japan Society for the Promotion of Science grants JP17H05884, JP20H05446, JP20H03226, JP17H06434, JP19H05784, and JP19H05781. Japan Agency for Medical Research and Development grant . Japan Science and Technology Agency, Precursory Research for Embryonic Science and Technology grants JPMJPR18G8 and JPMJPR16P1.