Serial crystallography captures dynamic control of sequential electron and proton transfer events in a flavoenzyme

Manuel Maestre-Reyna, Cheng Han Yang, Eriko Nango, Wei Cheng Huang, Eka Putra Gusti Ngurah Putu, Wen Jin Wu, Po Hsun Wang, Sophie Franz-Badur, Martin Saft, Hans Joachim Emmerich, Hsiang Yi Wu, Cheng Chung Lee, Kai Fa Huang, Yao Kai Chang, Jiahn Haur Liao, Jui Hung Weng, Wael Gad, Chiung Wen Chang, Allan H. Pang, Michihiro SugaharaShigeki Owada, Yuhei Hosokawa, Yasumasa Joti, Ayumi Yamashita, Rie Tanaka, Tomoyuki Tanaka, Fangjia Luo, Kensuke Tono, Kai Cheng Hsu, Stephan Kiontke, Igor Schapiro, Roberta Spadaccini, Antoine Royant, Junpei Yamamoto, So Iwata, Lars Oliver Essen*, Yoshitaka Bessho*, Ming Daw Tsai*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

16 Scopus citations

Abstract

Flavin coenzymes are universally found in biological redox reactions. DNA photolyases, with their flavin chromophore (FAD), utilize blue light for DNA repair and photoreduction. The latter process involves two single-electron transfers to FAD with an intermittent protonation step to prime the enzyme active for DNA repair. Here we use time-resolved serial femtosecond X-ray crystallography to describe how light-driven electron transfers trigger subsequent nanosecond-to-microsecond entanglement between FAD and its Asn/Arg-Asp redox sensor triad. We found that this key feature within the photolyase-cryptochrome family regulates FAD re-hybridization and protonation. After first electron transfer, the FAD•− isoalloxazine ring twists strongly when the arginine closes in to stabilize the negative charge. Subsequent breakage of the arginine–aspartate salt bridge allows proton transfer from arginine to FAD•−. Our molecular videos demonstrate how the protein environment of redox cofactors organizes multiple electron/proton transfer events in an ordered fashion, which could be applicable to other redox systems such as photosynthesis. [Figure not available: see fulltext.]

Original languageAmerican English
Pages (from-to)677-685
Number of pages9
JournalNature Chemistry
Volume14
Issue number6
DOIs
StatePublished - Jun 2022

Bibliographical note

Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature Limited.

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