Theory and Simulation of the Environmental Effects on FMO Electronic Transitions

Overview

Journal J Phys Chem Lett

Publisher American Chemical Society

Specialty Chemistry

Date 2011 Aug 2

PMID 21804928

Citations 32

Authors

Carsten Olbrich

Johan Strumpfer

Klaus Schulten

Ulrich Kleinekathofer

Affiliations

Soon will be listed here.

Abstract

Long-lived quantum coherence has been experimentally observed in the Fenna-Matthews-Olson (FMO) light-harvesting complex. It is much debated which role thermal effects play and if the observed low-temperature behavior arises also at physiological temperature. To contribute to this debate we use molecular dynamics simulations to study the coupling between the protein environment and the vertical excitation energies of individual bacteriochlorophyll molecules in the FMO complex of the green sulphur bacterium Chlorobaculum tepidum. The so-called spectral densities, which account for the environmental influence on the excited state dynamics, are determined from temporal autocorrelation functions of the energy gaps between ground and first excited states of the individual pigments. Although the overall shape of the spectral density is found to be rather similar for all pigments, variations in their magnitude can be seen. Differences between the spectral densities for the pigments of the FMO monomer and FMO trimer are also presented.

Citing Articles

Temporal witnesses of non-classicality in a macroscopic biological system.

Di Pietra G, Vedral V, Marletto C Sci Rep. 2024; 14(1):20094.

PMID: 39209858 PMC: 11362292. DOI: 10.1038/s41598-024-66159-x.

Mapping electronic decoherence pathways in molecules.

Gustin I, Kim C, McCamant D, Franco I Proc Natl Acad Sci U S A. 2023; 120(49):e2309987120.

PMID: 38015846 PMC: 10710033. DOI: 10.1073/pnas.2309987120.

Thermal site energy fluctuations in photosystem I: new insights from MD/QM/MM calculations.

Reiter S, Kiss F, Hauer J, de Vivie-Riedle R Chem Sci. 2023; 14(12):3117-3131.

PMID: 36970098 PMC: 10034153. DOI: 10.1039/d2sc06160k.

Recent progress in atomistic modeling of light-harvesting complexes: a mini review.

Maity S, Kleinekathofer U Photosynth Res. 2022; 156(1):147-162.

PMID: 36207489 PMC: 10070314. DOI: 10.1007/s11120-022-00969-w.

Predicting the future of excitation energy transfer in light-harvesting complex with artificial intelligence-based quantum dynamics.

Ullah A, Dral P Nat Commun. 2022; 13(1):1930.

PMID: 35411054 PMC: 9001686. DOI: 10.1038/s41467-022-29621-w.

References

Tronrud D, Wen J, Gay L, Blankenship R . The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosynth Res. 2009; 100(2):79-87. DOI: 10.1007/s11120-009-9430-6. View

Dijkstra A, Jansen T, Knoester J . Localization and coherent dynamics of excitons in the two-dimensional optical spectrum of molecular J-aggregates. J Chem Phys. 2008; 128(16):164511. DOI: 10.1063/1.2897753. View

Nazir A . Correlation-dependent coherent to incoherent transitions in resonant energy transfer dynamics. Phys Rev Lett. 2009; 103(14):146404. DOI: 10.1103/PhysRevLett.103.146404. View

Jansen T, Knoester J . Waiting time dynamics in two-dimensional infrared spectroscopy. Acc Chem Res. 2009; 42(9):1405-11. DOI: 10.1021/ar900025a. View

Wanko M, Hoffmann M, Strodel P, Koslowski A, Thiel W, Neese F . Calculating absorption shifts for retinal proteins: computational challenges. J Phys Chem B. 2006; 109(8):3606-15. DOI: 10.1021/jp0463060. View

Ishizaki A, Fleming G . Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature. Proc Natl Acad Sci U S A. 2009; 106(41):17255-60. PMC: 2762676. DOI: 10.1073/pnas.0908989106. View

Cho M, Vaswani H, Brixner T, Stenger J, Fleming G . Exciton analysis in 2D electronic spectroscopy. J Phys Chem B. 2006; 109(21):10542-56. DOI: 10.1021/jp050788d. View

Janosi L, Kosztin I, Damjanovic A . Theoretical prediction of spectral and optical properties of bacteriochlorophylls in thermally disordered LH2 antenna complexes. J Chem Phys. 2006; 125(1):014903. DOI: 10.1063/1.2210481. View

Brixner T, Stenger J, Vaswani H, Cho M, Blankenship R, Fleming G . Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature. 2005; 434(7033):625-8. DOI: 10.1038/nature03429. View

10.

Adolphs J, Renger T . How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria. Biophys J. 2006; 91(8):2778-97. PMC: 1578489. DOI: 10.1529/biophysj.105.079483. View

11.

Zucchelli G, Jennings R, Garlaschi F, Cinque G, Bassi R, Cremonesi O . The calculated in vitro and in vivo chlorophyll a absorption bandshape. Biophys J. 2001; 82(1 Pt 1):378-90. PMC: 1302477. DOI: 10.1016/S0006-3495(02)75402-7. View

12.

Kubar T, Kleinekathofer U, Elstner M . Solvent fluctuations drive the hole transfer in DNA: a mixed quantum-classical study. J Phys Chem B. 2009; 113(39):13107-17. DOI: 10.1021/jp9073587. View

13.

Abramavicius D, Mukamel S . Quantum oscillatory exciton migration in photosynthetic reaction centers. J Chem Phys. 2010; 133(6):064510. DOI: 10.1063/1.3458824. View

14.

Damjanovic A, Kosztin I, Kleinekathofer U, Schulten K . Excitons in a photosynthetic light-harvesting system: a combined molecular dynamics, quantum chemistry, and polaron model study. Phys Rev E Stat Nonlin Soft Matter Phys. 2002; 65(3 Pt 1):031919. DOI: 10.1103/PhysRevE.65.031919. View

15.

Wen J, Zhang H, Gross M, Blankenship R . Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting. Proc Natl Acad Sci U S A. 2009; 106(15):6134-9. PMC: 2669346. DOI: 10.1073/pnas.0901691106. View

16.

Tronrud D, Schmid M, Matthews B . Structure and X-ray amino acid sequence of a bacteriochlorophyll A protein from Prosthecochloris aestuarii refined at 1.9 A resolution. J Mol Biol. 1986; 188(3):443-54. DOI: 10.1016/0022-2836(86)90167-1. View

17.

Jansen T, Knoester J . Nonadiabatic effects in the two-dimensional infrared spectra of peptides: application to alanine dipeptide. J Phys Chem B. 2006; 110(45):22910-6. DOI: 10.1021/jp064795t. View

18.

Panitchayangkoon G, Hayes D, Fransted K, Caram J, Harel E, Wen J . Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc Natl Acad Sci U S A. 2010; 107(29):12766-70. PMC: 2919932. DOI: 10.1073/pnas.1005484107. View

19.

Ceccarelli M, Procacci P, Marchi M . An ab initio force field for the cofactors of bacterial photosynthesis. J Comput Chem. 2002; 24(2):129-42. DOI: 10.1002/jcc.10198. View

20.

Shim S, Rebentrost P, Valleau S, Aspuru-Guzik A . Atomistic study of the long-lived quantum coherences in the Fenna-Matthews-Olson complex. Biophys J. 2012; 102(3):649-60. PMC: 3274801. DOI: 10.1016/j.bpj.2011.12.021. View