Characterization of the Strongly Coupled, Low-Frequency Vibrational Modes of the Special Pair of Photosynthetic Reaction Centers via Isotopic Labeling of the Cofactors

Czarnecki, Kazimierz; Diers, James R.; Chynwat, Veeradej; Erickson, Joy; Frank, and Harry A.; Bocian, David F.

doi:10.1021/ja963281c

Cited by 74 publications

(138 citation statements)

References 79 publications

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“…It is important to realize, that if a change in the protein-cofactor coupling affects a vibrational mode significantly, then the protein must take part in the vibration. Therefore, our findings imply that chromophore-driven motions of the protein moiety play an important role in these low frequency vibrations, and they do not lend support to proposals that they are essentially cofactor modes (10,11).…”

Section: Discussioncontrasting

confidence: 99%

“…Recently, Czarnecki et al (11) investigated the geometry of the low frequency vibrations by using isotope substitution of the N and Mg atoms of P and by theoretical modeling of a Bchl monomer. The model included an imidazole ligated to the Mg atom, to simulate the histidine axial ligand associated with all of the RC Bchls, but did not include any additional protein matrix.…”

Section: Discussionmentioning

confidence: 99%

“…Their low frequency (mostly Ͻ250 cm Ϫ1 ) suggests that they are delocalized over the protein environment to a certain extent. However, Raman-active low frequency modes have been interpreted as being essentially localized in the Bchl macrocycle (10,11) and the coordinating histidine axial ligand (12). We previously have studied coherent nuclear motion in RCs with mutations in the residue Tyr-M210 (13), which is located within van der Waals distance of P, H L , and the intervening monomeric Bchl, B L. This residue is not directly bonded to any of these cofactors but is thought to influence their electronic interaction.…”

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confidence: 99%

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Low frequency vibrational modes in proteins: Changes induced by point-mutations in the protein-cofactor matrix of bacterial reaction centers

Rischel

Spiedel

Ridge

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

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As a step toward understanding their functional role, the low frequency vibrational motions (<300 cm ؊1 ) that are coupled to optical excitation of the primary donor bacteriochlorophyll cofactors in the reaction center from Rhodobacter sphaeroides were investigated. The pattern of hydrogen-bonding interaction between these bacteriochlorophylls and the surrounding protein was altered in several ways by mutation of single amino acids. The spectrum of low frequency vibrational modes identified by femtosecond coherence spectroscopy varied strongly between the different reaction center complexes, including between different mutants where the pattern of hydrogen bonds was the same. It is argued that these variations are primarily due to changes in the nature of the individual modes, rather than to changes in the charge distribution in the electronic states involved in the optical excitation. Pronounced effects of point mutations on the low frequency vibrational modes active in a proteincofactor system have not been reported previously. The changes in frequency observed indicate a strong involvement of the protein in these nuclear motions and demonstrate that the protein matrix can increase or decrease the f luctuations of the cofactor along specific directions.Any fundamental description of a biological process must ultimately encompass an account of small and possibly large scale changes in the nuclear geometry of the participating molecules. In particular, a central element in the determination of reaction efficiencies is the structure and accessibility of the transition state, which is the highest point on the free energy barrier that opposes changes in nuclear geometry as the system moves from reactant to product state. For proteins, atoms are most easily displaced along the ''soft'' directionsthe delocalized, low frequency modes-and the study of such motion during a reaction is therefore of particular interest.In recent years, a new aspect of low frequency motion has been revealed by the observation of coherent nuclear motion, persisting on the picosecond (ps) timescale following impulsive optical excitation, and manifested as oscillations in the transient optical properties of the protein cofactors. The discovery of this phenomenon in a variety of protein-cofactor systems, including the bacterial reaction center (RC) (1, 2), bacteriorhodopsin (3), and heme proteins (4), implies that ultrafast biological processes can occur on a timescale that is faster than vibrational relaxation (5). Therefore the possibility of coherent (in addition to thermal) motion along the reaction coordinate must be included in any complete description of a reaction. In addition, the measurement of oscillations by using femtosecond (fs) transient spectroscopy provides a new and convenient method for probing the spectrum of low frequency, nuclear vibrations that are set in motion by a physiological trigger. This study is aimed at assessing the factors that influence the character of such nuclear motions, by exploiting the possibil...

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Low frequency vibrational modes in proteins: Changes induced by point-mutations in the protein-cofactor matrix of bacterial reaction centers

Rischel

Spiedel

Ridge

et al. 1998

Proc. Natl. Acad. Sci. U.S.A.

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“…30 The frequency components of this spectral motion have been assigned to intramolecular vibrational modes within the chromophores, although the 40 cm À1 feature has been attributed either to phonon modes or vibrations of BChl a's acetyl tail. [31][32][33][34] Because the coherence time domain only accesses coherent superpositions of vibrational states on the excited-state surface (see the Experimental Procedure for further discussion), these frequency fluctuations are attributed to the excited-state vibrational motions. As a result of their delocalization, phonon modes may have an impact on the excitons collectively; but local vibrational motions should not.…”

Section: Resultsmentioning

confidence: 99%

Correlated Protein Environments Drive Quantum Coherence Lifetimes in Photosynthetic Pigment-Protein Complexes

Rolczynski

Zheng

Singh

et al. 2018

Chem

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Energy transfer in photosynthesis occurs as electronic excitations of coupled chromophores interact with their environment. The microscopic nature of these motions can enable novel energy-transfer mechanisms if the motions are not random. This study reveals synchronized and correlated fluctuations of the states within a photosynthetic pigment-protein complex, which explains prior observations of long-lived quantum coherence. SUMMARYEarly reports of long-lived quantum beating signals in photosynthetic pigmentprotein complexes were interpreted to suggest that electronic coherence benefits from protection by the protein, but many subsequent studies have suggested instead that vibrational or vibronic contributions are responsible for the observed signals. Here, we devised two 2D-spectroscopy methods to observe how each exciton is perturbed by its nuclear environment in a photosynthetic complex. The first approach simultaneously monitors each exciton's energy fluctuations over time to obtain its time-dependent electronic-nuclear interactions. The second method isolates evidence of coupled interexcitonic environmental motions. The techniques are validated with Nile Blue A and subsequently used on the Fenna-Matthews-Olson (FMO) complex. The FMO data reveal that each exciton experiences nearly identical spectral motion after excitation and that spectral motion of one excited exciton induces similar motion on unpopulated neighboring excitonic states. These synchronized and correlated spectral dynamics prolong coherences in the FMO complex after femtosecond excitation.

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“…Low frequency intermolecular modes that involve relative motion between the two pigments play a role in electron transfer within bacterial reaction centers; 29,58 such modes primarily affect the coupling coordinate. What makes energy transfer in a photosynthetic dimer different from a conical funnel 26,27 problem is that motions of the pigments necessary to reduce their coupling to zero (for example, in the transition dipole coupling approximation, the pigments must rotate so that their coupling becomes zero) do not appear to be energetically feasible while the pigments remain in the protein.…”

Section: Ab D = ∇J(q) Which Intramolecular Vibrations Contribute Tomentioning

confidence: 99%

Electronic energy transfer through non-adiabatic vibrational-electronic resonance. I. Theory for a dimer

Tiwari

Jonas

2017

The Journal of Chemical Physics

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Non-adiabatic vibrational-electronic resonance in the excited electronic states of natural photosynthetic antennas drastically alters the adiabatic framework, in which electronic energy transfer has been conventionally studied, and suggests the possibility of exploiting non-adiabatic dynamics for directed energy transfer. Here, a generalized dimer model incorporates asymmetries between pigments, coupling to the environment, and the doubly excited state relevant for nonlinear spectroscopy. For this generalized dimer model, the vibrational tuning vector that drives energy transfer is derived and connected to decoherence between singly excited states. A correlation vector is connected to decoherence between the ground state and the doubly excited state. Optical decoherence between the ground and singly excited states involves linear combinations of the correlation and tuning vectors. Excitonic coupling modifies the tuning vector. The correlation and tuning vectors are not always orthogonal, and both can be asymmetric under pigment exchange, which affects energy transfer. For equal pigment vibrational frequencies, the nonadiabatic tuning vector becomes an anti-correlated delocalized linear combination of intramolecular vibrations of the two pigments, and the nonadiabatic energy transfer dynamics become separable. With exchange symmetry, the correlation and tuning vectors become delocalized intramolecular vibrations that are symmetric and antisymmetric under pigment exchange. Diabatic criteria for vibrational-excitonic resonance demonstrate that anti-correlated vibrations increase the range and speed of vibronically resonant energy transfer (the Golden Rule rate is a factor of 2 faster). A partial trace analysis shows that vibronic decoherence for a vibrational-excitonic resonance between two excitons is slower than their purely excitonic decoherence.

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Characterization of the Strongly Coupled, Low-Frequency Vibrational Modes of the Special Pair of Photosynthetic Reaction Centers via Isotopic Labeling of the Cofactors

Cited by 74 publications

References 79 publications

Low frequency vibrational modes in proteins: Changes induced by point-mutations in the protein-cofactor matrix of bacterial reaction centers

Low frequency vibrational modes in proteins: Changes induced by point-mutations in the protein-cofactor matrix of bacterial reaction centers

Correlated Protein Environments Drive Quantum Coherence Lifetimes in Photosynthetic Pigment-Protein Complexes

Electronic energy transfer through non-adiabatic vibrational-electronic resonance. I. Theory for a dimer

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