Abstract
Time-resolved optical spectroscopy is widely used to study vibrational and electronic dynamics by monitoring transient changes in excited state populations on a femtosecond timescale1. Yet the fundamental cause of electronic and vibrational dynamics—the coupling between the different energy levels involved—is usually inferred only indirectly. Two-dimensional femtosecond infrared spectroscopy based on the heterodyne detection of three-pulse photon echoes2,3,4,5,6,7 has recently allowed the direct mapping of vibrational couplings, yielding transient structural information. Here we extend the approach to the visible range3,8 and directly measure electronic couplings in a molecular complex, the Fenna–Matthews–Olson photosynthetic light-harvesting protein9,10. As in all photosynthetic systems, the conversion of light into chemical energy is driven by electronic couplings that ensure the efficient transport of energy from light-capturing antenna pigments to the reaction centre11. We monitor this process as a function of time and frequency and show that excitation energy does not simply cascade stepwise down the energy ladder. We find instead distinct energy transport pathways that depend sensitively on the detailed spatial properties of the delocalized excited-state wavefunctions of the whole pigment–protein complex.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Zewail, A. H. Femtochemistry (World Scientific, Singapore, 1994)
Asplund, M. C., Zanni, M. T. & Hochstrasser, R. M. Two-dimensional infrared spectroscopy of peptides by phase-controlled femtosecond vibrational photon echoes. Proc. Natl Acad. Sci. USA 97, 8219–8224 (2000)
Mukamel, S. Multidimensional femtosecond correlation spectroscopies of electronic and vibrational excitations. Annu. Rev. Phys. Chem. 51, 691–729 (2000)
Wright, J. C. Coherent multidimensional vibrational spectroscopy. Int. Rev. Phys. Chem. 21, 185–255 (2002)
Khalil, M., Demirdöven, N. & Tokmakoff, A. Coherent 2D IR spectroscopy: Molecular structure and dynamics in solution. J. Phys. Chem. A 107, 5258–5279 (2003)
Asbury, J. B. et al. Hydrogen bond dynamics probed with ultrafast infrared heterodyne-detected multidimensional vibrational stimulated echoes. Phys. Rev. Lett. 91, 237402 (2003)
Cervetto, V., Helbing, J., Bredenbeck, J. & Hamm, P. Double-resonance versus pulsed Fourier transform two-dimensional infrared spectroscopy: An experimental and theoretical comparison. J. Chem. Phys. 121, 5935–5942 (2004)
Jonas, D. M. Two-dimensional femtosecond spectroscopy. Annu. Rev. Phys. Chem. 54, 425–463 (2003)
Fenna, R. E. & Matthews, B. W. Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola. Nature 258, 573–577 (1975)
Li, Y.-F., Zhou, W., Blankenship, R. E. & Allen, J. P. Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. J. Mol. Biol. 271, 456–471 (1997)
Blankenship, R. E. Molecular Mechanisms of Photosynthesis (Blackwell, Oxford, 2002)
Blankenship, R. E. & Matsuura, K. in Light-Harvesting Antennas in Photosynthesis (eds Green, B. R. & Parson, W. W.) 195–217 (Kluwer Academic, Dordrecht, 2003)
Savikhin, S., Buck, D. R. & Struve, W. S. Toward level-to-level energy transfers in photosynthesis: The Fenna–Matthews–Olson protein. J. Phys. Chem. B 102, 5556–5565 (1998)
Vulto, S. I. E. et al. Exciton simulations of optical spectra of the FMO complex from the green sulfur bacterium Chlorobium tepidum at 6 K. J. Phys. Chem. B 102, 9577–9582 (1998)
Vulto, S. I. E. et al. Excited state dynamics in FMO antenna complexes from photosynthetic green sulfur bacteria: A kinetic model. J. Phys. Chem. B 103, 8153–8161 (1999)
Wendling, M. et al. The quantitative relationship between structure and polarized spectroscopy in the FMO complex of Prosthecochloris aestuarii: Refining experiments and simulations. Photosynth. Res. 71, 99–123 (2002)
Lepetit, L. & Joffre, M. Two-dimensional nonlinear optics using Fourier-transform spectral interferometry. Opt. Lett. 21, 564–566 (1996)
Tian, P., Keusters, D., Suzaki, Y. & Warren, W. S. Femtosecond phase-coherent two-dimensional spectroscopy. Science 300, 1553–1555 (2003)
Cowan, M. L., Ogilvie, J. P. & Miller, R. J. D. Two-dimensional spectroscopy using diffractive optics based phased-locked photon echoes. Chem. Phys. Lett. 386, 184–189 (2004)
Brixner, T., Stopkin, I. V. & Fleming, G. R. Tunable two-dimensional femtosecond spectroscopy. Opt. Lett. 29, 884–886 (2004)
Brixner, T., Mancal, T., Stopkin, I. V. & Fleming, G. R. Phase-stabilized two-dimensional electronic spectroscopy. J. Chem. Phys. 121, 4221–4236 (2004)
Cho, M. Nonlinear response functions for three-dimensional spectroscopies. J. Chem. Phys. 115, 4424–4437 (2001)
Prall, B. S., Parkinson, D. Y., Fleming, G. R., Yang, M. & Ishikawa, N. Two-dimensional optical spectroscopy: Two-color photon echoes of electronically coupled phthalocyanine dimers. J. Chem. Phys. 120, 2537–2540 (2004)
Tokmakoff, A. Two-dimensional line shapes derived from coherent third-order nonlinear spectroscopy. J. Phys. Chem. A 104, 4247–4255 (2000)
Kwac, K. & Cho, M. Two-color pump-probe spectroscopies of two- and three-level systems: Two-dimensional line shapes and solvation dynamics. J. Phys. Chem. A 107, 5903–5912 (2003)
Zhang, W. M., Meier, T., Chernyak, V. & Mukamel, S. Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J. Chem. Phys. 108, 7763–7774 (1998)
Yang, M., Damjanovic, A., Vaswani, H. M. & Fleming, G. R. Energy transfer in photosystem I of cyanobacteria Synechococcus elongatus: Model study with structure-based semi-empirical Hamiltonian and experimental spectral density. Biophys. J. 85, 140–158 (2003)
van Amerongen, H., Valkunas, L. & van Grondelle, R. Photosynthetic Excitons (World Scientific, Singapore, 2000)
Maznev, A. A., Nelson, K. A. & Rogers, T. A. Optical heterodyne detection of laser-induced gratings. Opt. Lett. 23, 1319–1321 (1998)
Goodno, G. D., Dadusc, G. & Miller, R. J. D. Ultrafast heterodyne-detected transient-grating spectroscopy using diffractive optics. J. Opt. Soc. Am. B 15, 1791–1794 (1998)
Acknowledgements
We thank Y.-Z. Ma, L. Valkunas and M. Yang for discussions, and C. Goodhope for protein purification. The apparatus for 2D spectroscopy was constructed by I. V. Stiopkin and T.B. This work was supported by the DOE (at LBNL, UC Berkeley and Arizona State University), and by a CRIP grant to M.C. by KOSEF (Korea). T.B. thanks the German Science Foundation (DFG) for an Emmy Noether fellowship, and J.S. thanks the German Academic Exchange Service (DAAD) for a postdoctoral fellowship.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Rights and permissions
About this article
Cite this article
Brixner, T., Stenger, J., Vaswani, H. et al. Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434, 625–628 (2005). https://doi.org/10.1038/nature03429
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature03429
This article is cited by
-
Need of Quantum Biology to Investigate Beneficial Effects at Low Doses (< 100 mSv) and Maximize Peaceful Applications of Nuclear Energy
MAPAN (2024)
-
Optical two-dimensional coherent spectroscopy of excitons in transition-metal dichalcogenides
Frontiers of Physics (2024)
-
Filming enhanced ionization in an ultrafast triatomic slingshot
Communications Chemistry (2023)
-
Progress and prospects in nonlinear extreme-ultraviolet and X-ray optics and spectroscopy
Nature Reviews Physics (2023)
-
Single-photon absorption and emission from a natural photosynthetic complex
Nature (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.