Ultrafast proton-coupled isomerization in the phototransformation of phytochrome

• Published in: Nature chemistry 2022-07, Vol.14 (7), p.823-830
• Main Authors: Yang, Yang, Stensitzki, Till, Sauthof, Luisa, Schmidt, Andrea, Piwowarski, Patrick, Velazquez Escobar, Francisco, Michael, Norbert, Nguyen, Anh Duc, Szczepek, Michal, Brünig, Florian Nikolas, Netz, Roland Rüdiger, Mroginski, Maria Andrea, Adam, Suliman, Bartl, Franz, Schapiro, Igor, Hildebrandt, Peter, Scheerer, Patrick, Heyne, Karsten
• Format: Article
• Language: English
• Subjects: 631/45; 631/57; 631/92; 639/638; Analytical Chemistry; Biliverdin; Biochemistry; Chemistry; Chemistry and Materials Science; Chemistry/Food Science; Chromophores; Electric fields; Excitation; Hydrogen bonding; Hydrogen bonds; Inorganic Chemistry; Isomerization; Organic Chemistry; Oscillations; Physical Chemistry; Phytochromes; Plant growth; Protein structure; Proteins; Protons; Quantum mechanics
• ISSN: 1755-4330; 1755-4349
• DOI: 10.1038/s41557-022-00944-x

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. Phytochromes regulate plant growth by sensing far-red light through the photoisomerization of their protein-bound chromophores. In the phytochrome Agp2, it has now been demonstrated that ultrafast proton-transfer occurs from the chromophore to a protein–water network before photoisomerization, inducing protein changes on the ultrafast timescale. These protein changes develop further on longer timescales, resulting in an activated protein conformation.