Ultrafast dynamics and structural studies of prokaryotic and plant phytochromes

Principal Investigators: Prof. Dr. Karsten Heyne (FU), Prof. Dr. Jon Hughes (JLU)

Using X-ray crystallography together with state-of-the-art ultrafast Vis and IR spectroscopic methods, we propose to determine and interpret phytochrome structures and track ultrafast changes in hydrogen bonding networks, proton donor and acceptor groups and electrostatic interactions following photon absorption. We will focus on Cph1 and plant phytochromes, although studies on rhodopsins are also included. Comparison of related structures and dynamics will allow us to make general conclusions regarding structure/functional regulation via protonation dynamics and other processes.

Publications

2021 - 2024

Heyne, K. (2022). Impact of Ultrafast Electric Field Changes on Photoreceptor Protein Dynamics. J Phys Chem B. doi: 10.1021/acs.jpcb.1c08131.

Yang, Y., Stensitzki, T., Sauthof, L., Schmidt, A., Piwowarski, P., Velazquez Escobar, F., Michael, N., Nguyen, A.D., Szczepek, M., Brünig, F. N., Netz, R.R., Mroginski, M.A., Adam, S., Bartl, F.J., Schapiro, I., Hildebrandt, P., Scheerer, P., and Heyne, K. (2022). Ultrafast proton-coupled isomerization in the phototransformation of phytochrome. Nat Chem. doi: 10.1038/s41557-022-00944-x.

Zahn, C., Stensitzki, T. and Heyne, K. (2022). Femtosecond anisotropy excitation spectroscopy to disentangle the Qx and Qy absorption in chlorophyll a. Chemi Sci, 13, 42: 12426-12432. doi: 10.1039/D2SC03538C.

2017 - 2020

Kraskov, A., Nguyen, A.D., Goerling, J., Buhrke, D., Velazquez Escobar, F., Fernandez Lopez, M., Michael, N., Sauthof, L., Schmidt, A., Piwowarski, P., Yang, Y., Stensitzki, T., Adam, S., Bartl, F., Schapiro, I., Heyne, K., Siebert, F., Scheerer, P., Mroginski, M.A., and Hildebrandt, P. (2020). Intramolecular proton transfer controls protein structural changes in phytochrome. Biochemistry 59, 1023-1037. doi: 10.1021/acs.biochem.0c00053.

Nagano, S., Guan, K., Shenkutie, S., Feiler, C., Weiss, M. S., Kraskov, A., Buhrke, D., Hildebrandt, P., and Hughes, J. (2020). Structural insights into photoactivation and signalling in plant phytochromes. Nat Plants 6, 581-588. doi: 10.1038/s41477-020-0638-y.

Nass Kovacs, G., Colletier, J.-P., Grünbein, M. L., Yang, Y., Stensitzki, T., Batyuk, A., Carbajo, S., Doak, R. B., Ehrenberg, D., Foucar, L., Gasper, R., Gorel, A., Hilpert, M., Kloos, M., Koglin, J. E., Reinstein, J., Roome, C. M., Schlesinger, R., Seaberg, M., Shoeman, R. L., Stricker, M., Boutet, S., Haacke, S., Heberle, J., Heyne, K., Domratcheva, T., Barends, T. R. M., and Schlichting, I. (2019). Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin. Nature Communications 10, Article Number 3177. doi: 10.1038/s41467-019-10758.

Sadeghi, M., Balke, J., Schneider, C., Nagano, S., Stellmacher, J., Lochnit, G., Lang, C., Weise, C., Hughes, J., and Alexiev, U. (2020). Transient deprotonation of the chromophore affects protein dynamics proximal and distal to the linear tetrapyrrole chromophore in phytochrome Cph1. Biochemistry 59,1051-1062. doi: 10.1021/acs.biochem.9b00967.

Stensitzki, T., Adam, S., Schlesinger, R., Schapiro, I., and Heyne, K. (2020). Ultrafast backbone protonation in Channelrhodopsin-1 captured by polarization resolved fs vis-pump-IR-probe spectroscopy and computational methods. Molecules 25, pii: E848; doi: 10.3390/molecules25040848.

Stensitzki, T., Yang, Y., Wölke, A.L., Knapp, E.-W., Hughes, J., Mroginski, M. A., and Heyne, K. (2017). Influence of Heterogeneity on the Ultrafast Photoisomerization Dynamics of Pfr in Cph1 Phytochrome. Photochemistry and Photobiology 93, 703-712. doi: 10.1111/php.12743.

Velazquez Escobar, F., Buhrke, D., Lopez, M.F., Shenkutie, S.M., von Horsten, S., Essen, L.-O., Hughes, J. and Hildebrandt, P. (2017). Structural communication between the chromophore-binding pocket and the N-terminal extension in plant phytochrome phyB. FEBS Lett 591, 1258-1265. doi: 10.1002/1873-3468.12642.

Velazquez Escobar, F., Lang, C., Takiden, A., Schneider, C., Balke, J., Hughes, J., Alexiev, U., Hildebrandt, P. and Mroginski, M.A. (2017). Protonation-Dependent Structural Heterogeneity in the Chromophore Binding Site of Cyanobacterial Phytochrome Cph1. The Journal of Physical Chemistry B, 121, 1: 47-57. doi: 10.1021/acs.jpcb.6b09600.

2013 - 2016

Linke, M., Yang, Y., Zienicke, B., Hammam, M.A.S., von Haimberger, T., Zacarias, A., Inomata, K., Lamparter, T., and Heyne, K. (2013). Electronic transitions and heterogeneity of the bacteriophytochrome Pr absorption band: An angle balanced polarization resolved femtosecond VIS pump-IR probe study. Biophysical Journal 105, 1756-1766.

Stensitzki, T., Muders, V., Schlesinger, R., Heberle, J., and Heyne, K. (2015). The primary photoreaction of channelrhodopsin-1: Wavelength dependent photoreactions induced by ground-state heterogeneity. Frontiers in Molecular Biosciences 2, 41.

Stensitzki, T., Yang, Y., Berg, A., Mahammed, A., Gross, Z., and Heyne, K. (2016). Ultrafast electronic and vibrational dynamics in brominated aluminum corroles: Energy relaxation and triplet formation. Structural Dynamics 3, 043210.

Stensitzki, T., Yang, Y., Muders, V., Schlesinger, R., Heberle, J., and Heyne, K. (2016). Femtosecond infrared spectroscopy of channelrhodopsin-1 chromophore isomerization. Structural Dynamics 3, 043208.

Stöppler, D., Song, C., van Rossum, B.J., Geiger, M.A., Lang, C., Mroginski, M.A., Jagtap, A.P., Sigurdsson, S.T., Matysik, J., Hughes, J. and Oschkinat, H. (2016). Dynamic Nuclear Polarization Provides New Insights into Chromophore Structure in Phytochrome Photoreceptors. Angew Chem Int Ed Engl, 55, 52: 16017-16020. doi: 10.1002/anie.201608119.

Velazquez Escobar, F., von Stetten, D., Günther-Lütkens, M., Keidel, A., Michael, N., Lamparter, T., Essen, L.-O., Hughes, J., Gärtner, W., Yang, Y., Heyne, K., Mroginski, M.A., and Hildebrandt, P. (2015). Conformational heterogeneity of the Pfr chromophore in plant and cyanobacterial phytochromes. Frontiers in Molecular Biosciences 2, 37.

Yang, Y., Heyne, K., Mathies, R.A., and Dasgupta, J. (2016). Non-Bonded Interactions Drive the Sub-Picosecond Bilin Photoisomerization in the Pfr State of Phytochrome Cph1. ChemPhysChem 17, 369-374.

Yang, Y., Linke, M., von Haimberger, T., Matute, R., González, L., Schmieder, P., and Heyne, K. (2014). Active and silent chromophore isoforms for phytochrome Pr photoisomerization: An alternative evolutionary strategy to optimize photoreaction quantum yields. Structural Dynamics 1, 014701.