Molecular modeling of spectroscopy and quantum phenomena in light-harvesting complexes

• Applicant: Professor Dr. Ulrich Kleinekathöfer
• Subject Area: Theoretical Chemistry: Molecules, Materials, Surfaces ; Theoretical Chemistry: Electronic Structure, Dynamics, Simulation
• Term: from 2012 to 2016
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 226668712

• Final Report Year: 2018

Final Report Abstract

In most natural photosynthetic systems, light energy is absorbed by antenna pigment-protein complexes and subsequently transferred to a reaction center complex for conversion to a more stable form. The process of excitation energy transfer is an important step in photosynthesis and its detailed understanding might lead to improvements in efficiency for artificial photosynthetic systems. In this project light-harvesting (LH) complexes with an emphasis on the phycoerythrin 545 (PE545) photosynthetic antenna system of marine algae have been studied based on their atomic structure. After molecular dynamics simulations, excited state calculations of the chromophores were performed along the classical trajectories which describe the thermal motions of the nuclear positions within the respective LH complex. Comparing the environmental coupling to their respective protein environments, the major electronic transition in the PE545 and the Fenna-Matthews-Olson (FMO) complex show a rather similar energy-dependent behavior. Surprisingly, however, the molecular origin of these environmental couplings are quite different. While in case of the FMO complex, the coupling is indeed to the protein environment while in case of the PE545 aggregate the electronic transitions mainly couple to internal vibrations of the respective pigments. At the same time, these calculations allowed us to determine the exciton transfer dynamics which in none of the two mentioned complexes showed any oscillatory features. The exciton transfer times within the PE545 pigment-protein complex were compared to those of a very similar aggregate, namely the PE555 system. Both proteins consist of several parts and in the PE555 complex some parts are arranged differently leading to significantly longer exciton transfer times in comparison to those in PE545. This study clearly showed the importance of the spatial arrangements of the pigments for the excitation energy transfer. In another part of the project, we determined the dephasing time in the studied lightharvesting complexes. Dephasing and the corresponding dephasing times in light-harvesting complexes have been of quite some interest in recent years. Due to the quantum nature of energy and charge transfer processes, the effect of dephasing on these processes is of interest especially when trying to understand their efficiency. To this end, we studied the relationship between dephasing time and energy gap fluctuations of the individual molecular subunits and of the excitonic states. To our surprise, we found a clear relation for almost all studied complexes, i.e., an inverse relationship between dephasing times and energy gap fluctuations with the same prefactor. A theory was deviced explaining this finding based on the normalized energy gap autocorrelation functions. The effect of polarization in the force fields was investigated for the PE545 complex. Based on ensemble-averaged wave packet dynamics it was found that the effect of fluctuations in the couplings is small. At the same time, polarization effects do influence some of the inter-pigment couplings significantly while the excitation energy gaps are largely unaffected. In addition to these polarization effects, we also analyzed the effects of different force fields and quantum chemistry approaches on the above described results. Especially, the force fields of the pigments seem to influence the results considerably and thus a quantum treatment of the chromophores already during the dynamics seems to be in order in future work.

Publications

• Different Types of Vibrations Interacting with Electronic Excitations in Phycoerythrin 545 and Fenna- Matthews-Olson Antenna Systems, J. Phys. Chem. Lett. 5, 3131 (2014)
  M. Aghtar, J. Strümpfer, C. Olbrich, K. Schulten and U. Kleinekathöfer
  
• Influence of Force Fields and Quantum Chemistry Approach on Spectral Densities of BChl a in Solution and in FMO Proteins, J. Phys. Chem. B 119, 9995 (2015)
  S. Chandrasekaran, M. Aghtar, S. Valleau, A. Aspuru-Guzik and U. Kleinekathöfer
  
• Relation between Dephasing Time and Energy Gap Fluctuations in Biomolecular Systems, J. Phys. Chem. Lett. 7, 1102 (2016)
  M. I. Mallus, M. Aghtar, S. Chandrasekaran, G. L¨ demann, M. Elstner and U. Kleinekathöfer
  
• Impact of Electronic Fluctuations and Their Description on the Exciton Dynamics in the Light-Harvesting Complex PE545, J. Phys. Chem. B 121, 1330 (2017)
  M. Aghtar, U. Kleinekathöfer, C. Curutchet and B. Mennucci
  
• Protein Arrangement Effects on the Exciton Dynamics in the PE555 Complex, J. Phys. Chem. B 121, 3228 (2017)
  S. Chandrasekaran, K. R. Pothula and U. Kleinekathöfer
  
• Relation between Vibrational Dephasing Time and Energy Gap Fluctuations, J. Phys. Chem. B 121, 6471 (2017)
  M. I. Mallus, M. Schallwig and U. Kleinekathöfer