Origin of the multi-phasic quenching dynamics in the BLUF domains across the species

Yalin Zhou, Siwei Tang, Zijing Chen, Zhongneng Zhou, Jiulong Huang, Xiu-Wen Kang, Shuhua Zou, Bingyao Wang, Tianyi Zhang, Bei Ding () and Dongping Zhong ()
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Yalin Zhou: Shanghai Jiao Tong University
Siwei Tang: Shanghai Jiao Tong University
Zijing Chen: Shanghai Jiao Tong University
Zhongneng Zhou: Shanghai Jiao Tong University
Jiulong Huang: Shanghai Jiao Tong University
Xiu-Wen Kang: Shanghai Jiao Tong University
Shuhua Zou: Shanghai Jiao Tong University
Bingyao Wang: Shanghai Jiao Tong University
Tianyi Zhang: Shanghai Jiao Tong University
Bei Ding: Shanghai Jiao Tong University
Dongping Zhong: Shanghai Jiao Tong University

Nature Communications, 2024, vol. 15, issue 1, 1-11

Abstract: Abstract Blue light using flavin (BLUF) photoreceptors respond to light via one of nature’s smallest photo-switching domains. Upon photo-activation, the flavin cofactor in the BLUF domain exhibits multi-phasic dynamics, quenched by a proton-coupled electron transfer reaction involving the conserved Tyr and Gln. The dynamic behavior varies drastically across different species, the origin of which remains controversial. Here, we incorporate site-specific fluorinated Trp into three BLUF proteins, i.e., AppA, OaPAC and SyPixD, and characterize the percentages for the Wout, WinNHin and WinNHout conformations using 19F nuclear magnetic resonance spectroscopy. Using femtosecond spectroscopy, we identify that one key WinNHin conformation can introduce a branching one-step proton transfer in AppA and a two-step proton transfer in OaPAC and SyPixD. Correlating the flavin quenching dynamics with the active-site structural heterogeneity, we conclude that the quenching rate is determined by the percentage of WinNHin, which encodes a Tyr-Gln configuration that is not conducive to proton transfer.

Date: 2024
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DOI: 10.1038/s41467-023-44565-5

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