Andrew M. Moran

Vibronic enhancement of exciton sizes and energy transport in photosynthetic complexes.

Transport processes and spectroscopic phenomena in light harvesting proteins depend sensitively on the characteristics of electron-phonon couplings. Decoherence imposed by low-frequency nuclear motion generally suppresses the delocalization of electronic states, whereas the Franck-Condon progressions of high-frequency intramolecular modes underpin a hierarchy of vibronic Coulombic interactions between pigments. This Article investigates the impact of vibronic couplings on the electronic structures and relaxation mechanisms of two cyanobacterial light-harvesting proteins, allophycocyanin (APC) and C-phycocyanin (CPC). Both APC and CPC possess three pairs of pigments (i.e., dimers) that undergo electronic relaxation on the subpicosecond time scale. Electronic relaxation is ~10 times faster in APC than in CPC despite the nearly identical structures of their pigment dimers. We suggest that the distinct behaviors of these closely related proteins are understood on the same footing only in a basis of joint electronic-nuclear states (i.e., vibronic excitons). A vibronic exciton model predicts well-defined rate enhancements in APC at realistic values of the site reorganization energies, whereas a purely electronic exciton model points to faster dynamics in CPC. Calculated exciton sizes (i.e., participation ratios) show that wave function delocalization underlies the rate enhancement predicted by the vibronic exciton model. Strong vibronic coupling and heterogeneity in the pigment sites are the key ingredients of the vibronic delocalization mechanism. In contrast, commonly employed purely electronic exciton models see heterogeneity as only a localizing influence. This work raises the possibility that similar vibronic effects, which are often neglected, may generally have a significant influence on energy transport in molecular aggregates and photosynthetic complexes.

Concerted electron-proton transfer in the optical excitation of hydrogen-bonded dyes

The simultaneous, concerted transfer of electrons and protons—electron-proton transfer (EPT)—is an important mechanism utilized in chemistry and biology to avoid high energy intermediates. There are many examples of thermally activated EPT in ground-state reactions and in excited states following photoexcitation and thermal relaxation. Here we report application of ultrafast excitation with absorption and Raman monitoring to detect a photochemically driven EPT process (photo-EPT). In this process, both electrons and protons are transferred during the absorption of a photon. Photo-EPT is induced by intramolecular charge-transfer (ICT) excitation of hydrogen-bonded-base adducts with either a coumarin dye or 4-nitro-4′-biphenylphenol. Femtosecond transient absorption spectral measurements following ICT excitation reveal the appearance of two spectroscopically distinct states having different dynamical signatures. One of these states corresponds to a conventional ICT excited state in which the transferring H+ is initially associated with the proton donor. Proton transfer to the base (B) then occurs on the picosecond time scale. The other state is an ICT-EPT photoproduct. Upon excitation it forms initially in the nuclear configuration of the ground state by application of the Franck–Condon principle. However, due to the change in electronic configuration induced by the transition, excitation is accompanied by proton transfer with the protonated base formed with a highly elongated +H─B bond. Coherent Raman spectroscopy confirms the presence of a vibrational mode corresponding to the protonated base in the optically prepared state.

Exciton Coherence and Energy Transport in the Light-Harvesting Dimers of Allophycocyanin

Femtosecond transient grating and photon echo spectroscopies with a sub-20 fs time resolution are applied to allophycocyanin (APC), a protein located at the base of the phycobilisome antenna of cyanobacteria. Coupling between pairs of phycocyanobilin pigments with nondegenerate energy levels gives rise to the four-level exciton electronic structure of APC. Spectroscopic signals obtained in multiple experiments (e.g., linear absorption, fluorescence, transient grating, 2D Fourier transform photon echo) are used to constrain the parameters of a Frenkel exciton Hamiltonian. Comparison between experiment and theory yields a robust microscopic understanding of the electronic and nuclear relaxation dynamics. In agreement with previous work, transient absorption anisotropy establishes that internal conversion between the exciton states of the dimer occurs with time constants of 35, 220, and 280 fs. The sub-100 fs dynamics are decomposed into three distinct relaxation processes: electronic population transfer, intramolecular vibrational energy redistribution, and the dephasing of electronic and nuclear coherences. Model calculations show that the sub-100 fs red-shift in the transient absorption signal spectrum reflects interference between stimulated emission (ESE) and excited state absorption (ESA) signal components. It is also established that the pigment fluctuations in the dimer are not well-correlated, although further experiments will be required to precisely quantify the amount of correlation. The findings of this paper suggest that the light harvesting function of APC is enhanced by nondegeneracy of the pigments comprising the dimer and strong vibronic coupling of intramolecular modes on the phycocyanobilins. We find that the exciton states are 96% localized to the individual molecular sites within a particular dimer. Localization of the transition densities, in turn, is suggested to promote significant vibronic coupling which serves to both broaden the absorption line shape and open channels for fast internal conversion. The dominant internal conversion channel is assigned to a promoting mode near 800 cm(-1) involving hydrogen out-of-plane (HOOP) wagging motion similar to that observed in phytochrome and retinal. This rate enhancement ensures that all photoexcitations quickly and efficiently relax to the electronic origin of the lower energy exciton state from which energy transfer to the reaction center occurs.

Two-dimensional electronic spectroscopy in the ultraviolet wavelength range

Coherent two-dimensional (2D) spectroscopies conducted at visible and infrared wavelengths are having a transformative impact on the understanding of numerous processes in condensed phases. The extension of 2D spectroscopy to the ultraviolet spectral range (2DUV) must contend with several challenges, including the attainment of adequate laser bandwidth, interferometric phase stability, and the suppression of undesired nonlinearities in the sample medium. Solutions to these problems are motivated by the study of a wide range of biological systems whose lowest-frequency electronic resonances are found in the UV. The development of 2DUV spectroscopy also makes possible the attainment of new insights into elementary chemical reaction dynamics (e.g., electrocyclic ring opening in cycloalkenes). Substantial progress has been made in both the implementation and application of 2DUV spectroscopy in the past several years. In this Perspective, we discuss 2DUV methodology, review recent applications, and speculate on what the future will hold.

Linear and nonlinear infrared signatures of local α- and 310-helical structures in alanine polypeptides

Vibrational exciton Hamiltonians for the amide I and amide A modes of both the α- and 310-helical conformations of a fifteen unit polyalanine oligomer CH3–CO(Ala)15–NHCH3 are constructed using density-functional calculations for smaller model peptides. Energy levels as well as the transition dipoles of all singly and doubly excited-state manifolds are calculated. A variety of C13-substituted isotopic derivatives are examined with respect to their ability to reveal differences in local secondary structures in two-dimensional infrared spectra in the amide I region. Amide mode anharmonicities are predicted to be valid indicators of secondary helical structures.

Probing ultrafast dynamics in adenine with mid-UV four-wave mixing spectroscopies.

Heterodyne-detected transient grating (TG) and two-dimensional photon echo (2DPE) spectroscopies are extended to the mid-UV spectral range in this investigation of photoinduced relaxation processes of adenine in aqueous solution. These experiments are the first to combine a new method for generating 25 fs laser pulses (at 263 nm) with the passive phase stability afforded by diffractive optics-based interferometry. We establish a set of conditions (e.g., laser power density, solute concentration) appropriate for the study of dynamics involving the neutral solute. Undesired solute photoionization is shown to take hold at higher peak powers of the laser pulses. Signatures of internal conversion and vibrational cooling dynamics are examined using TG measurements with signal-to-noise ratios as high as 350 at short delay times. In addition, 2DPE line shapes reveal correlations between excitation and emission frequencies in adenine, which reflect electronic and nuclear relaxation processes associated with particular tautomers. Overall, this study demonstrates the feasibility of techniques that will hold many advantages for the study of biomolecules whose lowest-energy electronic resonances are found in the mid-UV (e.g., DNA bases, amino acids).

Ab initio simulation of the two-dimensional vibrational spectrum of dicarbonylacetylacetonato rhodium(I)

The complete anharmonic cubic and quartic force field of the two carbonyl stretching vibrations of a rhodium di-carbonyl complex is calculated at the density functional level and used to simulate the third-order vibrational response function. The infrared photon echo spectrum calculated using the diagonalized resulting exciton Hamiltonian is in qualitative agreement with measured values. Quartic terms in the potential are critical for reproducing the experimental transition energies and transition dipoles.

Infrared photon echo signatures of hydrogen bond connectivity in the cyclic decapeptide antamanide

Distinct hydrogen bonding patterns are predicted in the amide I and amide A vibrational bands of four dominant conformations of antamanide using anharmonic vibrational Hamiltonians constructed at the DFT and AM1 levels. We show how these conformations may be distinguished using coherent three pulse infrared measurements with several pulse polarization configurations in the amide I region. The amide A hydrogen bonded N–H stretching modes are highly localized and have conformation-dependent frequencies, but their anharmonicities are insensitive to local structure at the hydrogen bond distances in antamanide.

Nature of Excited States and Relaxation Mechanisms in C-Phycocyanin

The electronic structure and photoinduced relaxation dynamics of the cyanobacterial light harvesting protein, C-Phycocyanin (CPC), are examined using transient grating and two-dimensional (2D) photon echo spectroscopies possessing sub-20 fs time resolution. In combination with linear absorption and fluorescence measurements, these time-resolved experiments are used to constrain the parameters of a Frenkel exciton Hamiltonian. Particular emphasis is placed on elucidating the nature of excited states involving the alpha84 and beta84 phycocyanobilin pigment dimers of CPC. This paper obtains new experimental evidence suggesting that electronic relaxation proceeds by way of incoherent energy transfer between the alpha84 and beta84 pigment sites (i.e., the weak coupling limit of energy transfer). Transient absorption anisotropies simulated in the weak coupling limit agree well with measurements, whereas signals computed in an exciton basis possess short-lived (electronic) coherent components not present in the experimental data. In addition, 2D photon echo spectra for CPC show no sign of the interfering nonlinearities predicted by a theoretical model to be characteristic of exciton formation. Another important new observation is that the sub-100 fs dynamics in the transient absorption anisotropy are dominated by an impulsively excited hydrogen out-of-plane wagging mode similar to those observed in phytochrome and retinal. Detection of this 795 cm(-1) coherence is of particular interest because our recent study of a closely related protein, Allophycocyanin (APC), assigns a similar coordinate as a promoting mode enabling ultrafast internal conversion. Together, the experiments conducted for APC and CPC suggest that interactions between the pigments and environment are the key to understanding why electronic relaxation in CPC is more than three times slower than APC despite the nearly identical geometries of the pigment dimers. Most important in reaching this conclusion is the present finding that relaxation of the 2D photon echo line shapes of CPC is approximately two times faster than that measured for APC. Overall, the present results underscore the ability of phycobiliproteins to control light harvesting dynamics through solvation and variation in the conformations of open-chain tetrapyrrole chromophores.

Correlated exciton fluctuations in cylindrical molecular aggregates.

Femtosecond electronic relaxation dynamics of a cylindrical molecular aggregate are measured with transient grating (TG) and two-dimensional Fourier transform photon echo (PE) spectroscopies. The aggregates are double-walled cylindrical structures formed by self-assembly of amphiphilic cyanine dye molecules in water. The diameters of the inner and outer cylinders are approximately 6 and 10 nm. The linear absorption spectrum of the aggregate exhibits four spectrally resolved single exciton transitions corresponding to excited states localized on particular regions of the structure: (1) an excited state localized on the inner cylinder corresponds to the lowest energy transition at 16670 cm(-1); (2) a transition at 17150 cm(-1) represents a state localized on the outer cylinder, (3) whereas an overlapping peak found at 17330 cm(-1) is more closely associated with the inner cylinder; (4) an excited state delocalized between the inner and outer cylinder is assigned to a transition in the linear absorption spectrum at 17860 cm(-1). TG spectra show a series of resonances reflecting the electronic structure of both the single and double exciton manifolds. In addition, PE spectra reveal coherent modulation of both diagonal and cross-peak amplitudes persisting for 100 fs, where the coherence frequency matches the energy gap between transitions 1 and 4 in the linear absorption spectrum. PE line shapes suggest correlated energy level fluctuations for the exciton states associated with these two transitions, which is consistent with this fairly long-lasting coherence at room temperature in aqueous solution. The impact of these correlations on Forster energy transfer efficiency is discussed. The observations imply fairly long-range correlations between the molecular sites (>0.6 nm), which in turn reflects the length scale of the environmental motion inducing the fluctuations. We suggest that this environmental motion is most likely associated with water confined inside the cylinder and/or fluctuations of the dyes aliphatic functional groups.