Ultrafast proton-coupled isomerization in the phototransformation of phytochrome

Yang Yang, Till Stensitzki, Luisa Sauthof, Andrea Schmidt, Patrick Piwowarski, Francisco Velazquez Escobar, Norbert Michael, Anh Duc Nguyen, Michal Szczepek, Florian Nikolas Brünig, Roland Rüdiger Netz, Maria Andrea Mroginski, Suliman Adam, Franz Bartl, Igor Schapiro, Peter Hildebrandt, Patrick Scheerer, Karsten Heyne*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

9 Scopus citations

Abstract

The biological function of phytochromes is triggered by an ultrafast photoisomerization of the tetrapyrrole chromophore biliverdin between two rings denoted C and D. The mechanism by which this process induces extended structural changes of the protein is unclear. Here we report ultrafast proton-coupled photoisomerization upon excitation of the parent state (Pfr) of bacteriophytochrome Agp2. Transient deprotonation of the chromophore’s pyrrole ring D or ring C into a hydrogen-bonded water cluster, revealed by a broad continuum infrared band, is triggered by electronic excitation, coherent oscillations and the sudden electric-field change in the excited state. Subsequently, a dominant fraction of the excited population relaxes back to the Pfr state, while ~35% follows the forward reaction to the photoproduct. A combination of quantum mechanics/molecular mechanics calculations and ultrafast visible and infrared spectroscopies demonstrates how proton-coupled dynamics in the excited state of Pfr leads to a restructured hydrogen-bond environment of early Lumi-F, which is interpreted as a trigger for downstream protein structural changes. [Figure not available: see fulltext.].

Original languageAmerican English
Pages (from-to)823-830
Number of pages8
JournalNature Chemistry
Volume14
Issue number7
DOIs
StatePublished - Jul 2022

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