The interplay between chromophore and protein determines the extended excited state dynamics in a single-domain phytochrome
- 26 June 2020
- journal article
- research article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 117 (28), 16356-16362
- https://doi.org/10.1073/pnas.1921706117
Abstract
Phytochromes are a diverse family of bilin-binding photoreceptors that regulate a wide range of physiological processes. Their photochemical properties make them attractive for applications in optogenetics and superresolution microscopy. Phytochromes undergo reversible photoconversion triggered by the Z ⇄ E photoisomerization about the double bond in the bilin chromophore. However, it is not fully understood at the molecular level how the protein framework facilitates the complex photoisomerization dynamics. We have studied a single-domain bilin-binding photoreceptor All2699g1 (Nostoc sp. PCC 7120) that exhibits photoconversion between the red light-absorbing (Pr) and far red-absorbing (Pfr) states just like canonical phytochromes. We present the crystal structure and examine the photoisomerization mechanism of the Pr form as well as the formation of the primary photoproduct Lumi-R using time-resolved spectroscopy and hybrid quantum mechanics/molecular mechanics simulations. We show that the unusually long excited state lifetime (broad lifetime distribution centered at ∼300 picoseconds) is due to the interactions between the isomerizing pyrrole ring D and an adjacent conserved Tyr142. The decay kinetics shows a strongly distributed character which is imposed by the nonexponential protein dynamics. Our findings offer a mechanistic insight into how the quantum efficiency of the bilin photoisomerization is tuned by the protein environment, thereby providing a structural framework for engineering bilin-based optical agents for imaging and optogenetics applications.Keywords
Funding Information
- Deutsche Forschungsgemeinschaft (WA 1850/4-2)
- National Natural Science Foundation of China (31861143029, 44131770822)
- Foundation for the National Institutes of Health (R01EY024363)
This publication has 54 references indexed in Scilit:
- Smallest near-infrared fluorescent protein evolved from cyanobacteriochrome as versatile tag for spectral multiplexingNature Communications, 2019
- Phytochrome diversification in cyanobacteria and eukaryotic algaeCurrent Opinion in Plant Biology, 2017
- The family of phytochrome-like photoreceptors: diverse, complex and multi-colored, but very usefulCurrent Opinion in Structural Biology, 2015
- Engineering of a red-light–activated human cAMP/cGMP-specific phosphodiesteraseProceedings of the National Academy of Sciences, 2014
- Structure and Function of Plant PhotoreceptorsAnnual Review of Plant Biology, 2010
- Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteriaPhotochemical & Photobiological Sciences, 2008
- PHYTOCHROME STRUCTURE AND SIGNALING MECHANISMSAnnual Review of Plant Biology, 2006
- The Structure of Phytochrome: A Picture Is Worth a Thousand SpectraPlant Cell, 2005
- Phytochrome ancestry: sensors of bilins and lightTrends in Plant Science, 2002
- A Second Photochromic Bacteriophytochrome from Synechocystis sp. PCC 6803: Spectral Analysis and Down-Regulation by LightBiochemistry, 2000