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

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 ␣-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.energy transfer ͉ light-harvesting ͉ optical spectra ͉ photosynthesis ͉ structure-based simulation P hotosynthesis is the fundamental biological process in which solar energy is converted into biomass. The first step is the capture of light by arrays of protein-bound dye molecules (pigments). These pigment-protein complexes (PPCs) are therefore termed light-harvesting complexes or antenna proteins (1). They transfer the excitation energy with high quantum yield to specialized PPCs, the reaction centers, where the energy is used to trigger the chemical modification of substrates. To guide the excitation energy flow in a certain direction there has to be an energy sink, that is, the pigments in the target region are required to absorb at lower energies than the initially excited chromophores. A complication of this simple picture arises from long-range electrostatic interactions between the local excitations (excitonic couplings), which are a prerequisite for energy transfer. These couplings cause the excited states of the PPC (exciton states) to be delocalized, that is, their electronic wave functions contain contributions of several pigments in the complex. Directed energy transport results from energetic relaxation transferring population between exciton states of different spatial extents. The latter depend crucially on excitonic couplings and site energies, so that the elucidation of energy-transfer mechanisms on the basis of spectroscopic data (2-4) and crystal structures (5-7) requires knowledge of both these quantities (8, 9), which are not direct...

The feasibility of coherent energy transfer in microtubules

“…Site energies were derived from structure-based calculations of the free energy change of the protein-pigment complex (PPC) that occurs when the ground state charge density of Trp m is shifted to the first excited state, analogous to methods used for the FMO complex [26,61,62]. Quantum chemical calculations of the pigments in vacuo yield the charge distributions of the S 0 and 1L a states and a contribution DE qm to the S 0 !…”

“…As persistent electronic coherences may be a general property of any system of compact nearly static chromophores coupled to the environment [24], we investigate the biological feasibility of coherent energy transfer in the tubulin dimer. Via a combination of homology modelling, molecular dynamics (MD) simulations, quantum chemistry and optical biophysics, we apply structure-based simulations similar to current studies of the FMO complex [25,26], and larger LHCs [27] to probe potential energy transfer mechanisms in tubulin, and by extension microtubules.…”

Long-lived quantum coherence in photosynthetic complexes at physiological temperature

“…The FMO pigment-protein complex from Chlorobium tepidum serves as a model system for photosynthetic energy transfer processes (2,(10)(11)(12)(13). This complex conducts energy from the larger light-harvesting chlorosome to the reaction center in green sulfur bacteria (14,15).…”

Chlorophylls, Symmetry, Chirality, and Photosynthesis

“…As a result, numerous studies of the site-energy distributions and exciton dynamics have been reported [222], and have included explicit investigations of the influence of variations in BChl conformation [64,65,104,225]. So far, the best agreement between structure-based ab initio calculations of the site-energies with those empirically determined by parametric fitting to the experimental spectra, have been obtained by consideration of the effect of the electrostatic environments of the BChl binding-sites on the relative stabilities of their ground-and excited-states [226,227].…”