α-helices direct excitation energy flow in the Fenna-Matthews-Olson protein

Frank Müh, Mohamed Madjet, Julia Adolphs, Ayjamal Abdurahman, Björn Rabenstein, Hiroshi Ishikita, Ernst Walter Knapp, Thomas Renger

Research output: Contribution to journalArticle

153 Citations (Scopus)

Abstract

In photosynthesis, light is captured by antenna proteins. These proteins transfer the excitation energy with almost 100% quantum efficiency to the reaction centers, where charge separation takes place. The time scale and pathways of this transfer are controlled by the protein scaffold, which holds the pigments at optimal geometry and tunes their excitation energies (site energies). The detailed understanding of the tuning of site energies by the protein has been an unsolved problem since the first high-resolution crystal structure of a light-harvesting antenna appeared >30 years ago [Fenna RE, Matthews BW (1975) Nature 258:573-577]. Here, we present a combined quantum chemical/electrostatic approach to compute site energies that considers the whole protein in atomic detail and provides the missing link between crystallography and spectroscopy. The calculation of site energies of the Fenna-Matthews-Olson protein results in optical spectra that are in quantitative agreement with experiment and reveals an unexpectedly strong influence of the backbone of two α-helices. The electric field from the latter defines the direction of excitation energy flow in the Fenna-Matthews-Olson protein, whereas the effects of amino acid side chains, hitherto thought to be crucial, largely compensate each other. This result challenges the current view of how energy flow is regulated in pigment-protein complexes and demonstrates that attention has to be paid to the backbone architecture.

Original languageEnglish
Pages (from-to)16862-16867
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume104
Issue number43
DOIs
Publication statusPublished - 23 Oct 2007
Externally publishedYes

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Proteins
Light
Crystallography
Energy Transfer
Photosynthesis
Static Electricity
Spectrum Analysis
Amino Acids

Keywords

  • Energy transfer
  • Light-harvesting
  • Optical spectra
  • Photosynthesis
  • Structure-based simulation

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

α-helices direct excitation energy flow in the Fenna-Matthews-Olson protein. / Müh, Frank; Madjet, Mohamed; Adolphs, Julia; Abdurahman, Ayjamal; Rabenstein, Björn; Ishikita, Hiroshi; Knapp, Ernst Walter; Renger, Thomas.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, No. 43, 23.10.2007, p. 16862-16867.

Research output: Contribution to journalArticle

Müh, Frank ; Madjet, Mohamed ; Adolphs, Julia ; Abdurahman, Ayjamal ; Rabenstein, Björn ; Ishikita, Hiroshi ; Knapp, Ernst Walter ; Renger, Thomas. / α-helices direct excitation energy flow in the Fenna-Matthews-Olson protein. In: Proceedings of the National Academy of Sciences of the United States of America. 2007 ; Vol. 104, No. 43. pp. 16862-16867.
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