Abstract-Terahertz radiation induces non-thermal structural changes associated with Fröhlich condensation in a protein crystal

Ida V. Lundholm^1,a), Helena Rodilla^2,a), Weixiao Y. Wahlgren¹,Annette Duelli¹, Gleb Bourenkov³, Josip Vukusic², Ran Friedman⁴, Jan Stake², Thomas Schneider³ and Gergely Katona^1,b)


1 Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
2 Department of Microtechnology and Nanoscience, Chalmers University of Technology, Gothenburg, Sweden
3 European Molecular Biology Laboratory Hamburg Outstation, EMBL c/o DESY, Notkestrasse 85, 22603 Hamburg, Germany
4 Department of Chemistry and Biomedicinal Sciences and Centre for Biomaterials Chemistry, Linnaeus University, Kalmar, Sweden
a) I. V. Lundholm and H. Rodilla contributed equally to this work.
b) Author to whom correspondence should be addressed. Electronic mail:gergely.katona@cmb.gu.se
Struct. Dyn. 2, 054702 (2015); http://dx.doi.org/10.1063/1.4931825

http://scitation.aip.org/content/aca/journal/sdy/2/5/10.1063/1.4931825

Whether long-range quantum coherent states could exist in biological systems, and beyond low-temperature regimes where quantum physics is known to be applicable, has been the subject to debate for decades. It was proposed by Fröhlich that vibrational modes within proteinmolecules can order and condense into a lowest-frequency vibrational mode in a process similar to Bose-Einstein condensation, and thus that macroscopic coherence could potentially be observed in biological systems. Despite the prediction of these so-called Fröhlich condensates almost five decades ago, experimental evidence thereof has been lacking. Here, we present the first experimental observation of Fröhlich condensation in a protein structure. To that end, and to overcome the challenges associated with probing low-frequency molecular vibrations in proteins (which has hampered understanding of their role in proteins' function), we combined terahertz techniques with a highly sensitive X-ray crystallographic method to visualize low-frequency vibrational modes in the protein structure of hen-egg white lysozyme. We found that 0.4 THz electromagnetic radiation induces non-thermal changes in electron density. In particular, we observed a local increase of electron density in a long α-helix motif consistent with a subtle longitudinal compression of the helix. These observed electron density changes occur at a low absorption rate indicating that thermalization of terahertz photons happens on a micro- to milli-second time scale, which is much slower than the expected nanosecond time scale due to damping of delocalized low frequency vibrations. Our analyses show that the micro- to milli-second lifetime of the vibration can only be explained by Fröhlich condensation, a phenomenon predicted almost half a century ago, yet never experimentally confirmed.

Abstract-Terahertz Absorption of illuminated Photosynthetic Reaction Center solution: a signature of photoactivation?

Ida Veronica Lundholm,   Weixiao Yuan Wahlgren,  Federica Piccirilli,   Paola di Pietro,   Annette Duelli,  Oskar Berntsson,   Stefano Lupi,   Andrea Perucchi and  Gergely Katona  

RSC Adv., 2014, Accepted Manuscript

DOI: 10.1039/C4RA03787A
Accepted 27 May 2014
First published online 29 May 2014

http://pubs.rsc.org/en/content/articlelanding/2014/ra/c4ra03787a#!divAbstract

Photosynthetic reaction centers develop a stable charge separated state upon illumination. To investigate the molecular vibrations associated with the illuminated state of a reaction center we recorded terahertz absorption spectra of the photosynthetic reaction center from Rhodobacter sphaeroides in the dark and upon illumination and observed a small, but significant THz absorption increase in the 20 to 130 cm-1 spectral region. Reaction centers show very similar terahertz absorption increase when solubilized in detergents and in a lipidic sponge phase indicating that the nature of the bulk solvent has limited influence on the vibrational spectrum. The absorption change of the isolated LM subunit is very similar to that of the intact reaction center. Through temperature control experiments we show that 89 % of the absorption change is likely attributed to the non-thermal activation of the protein molecules. These results indicate that picosecond molecular vibrations change primarily in the cofactors and/or in the evolutionary conserved core of the reaction centre upon illumination, whereas the nuclear motions of the H-subunit and the bulk solvent have limited impact on the terahertz spectral changes.