Jessica M. Anna

Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms

The process of photosynthesis is initiated by the capture of sunlight by a network of light-absorbing molecules (chromophores), which are also responsible for the subsequent funneling of the excitation energy to the reaction centers. Through evolution, genetic drift, and speciation, photosynthetic organisms have discovered many solutions for light harvesting. In this review, we describe the underlying photophysical principles by which this energy is absorbed, as well as the mechanisms of electronic excitation energy transfer (EET). First, optical properties of the individual pigment chromophores present in light-harvesting antenna complexes are introduced, and then we examine the collective behavior of pigment-pigment and pigment-protein interactions. The description of energy transfer, in particular multichromophoric antenna structures, is shown to vary depending on the spatial and energetic landscape, which dictates the relative coupling strength between constituent pigment molecules. In the latter half of the article, we focus on the light-harvesting complexes of purple bacteria as a model to illustrate the present understanding of the synergetic effects leading to EET optimization of light-harvesting antenna systems while exploring the structure and function of the integral chromophores. We end this review with a brief overview of the energy-transfer dynamics and pathways in the light-harvesting antennas of various photosynthetic organisms.

Two-Dimensional Infrared Spectroscopy of Metal Carbonyls

Metal carbonyl complexes offer both rich chemistry and complex vibrational spectroscopy due to strong coupling among the carbonyl stretches. Using two-dimensional infrared (2DIR) spectroscopy, it is possible to resolve the underlying transitions between vibrational energy levels, determine the orientations and relative magnitude of the corresponding transition dipole moments, measure the coupling between modes due to the anharmonicity of the potential, and probe energy redistribution among the modes as well as energy relaxation to other degrees of freedom. Measurements on metal carbonyl complexes have played, and continue to play, a crucial role in facilitating the development of 2DIR spectroscopy. These compounds have provided powerful demonstrations of the unique ability of 2DIR spectroscopy to resolve vibrational structure and dynamics in multimode systems. In addition, invaluable new information has been obtained on metal-to-ligand charge transfer processes, solvent-solute interactions and fluxionality. Since transition metal complexes play important roles in catalysis and as dye sensitizers for semiconductor nanoparticle photocatalysis, detailed probes of equilibrium and phototriggered dynamics should aid our understanding of these key catalytic systems. The richness and level of detail provided by the 2DIR spectra of metal carbonyl complexes turn them into extremely useful model systems for testing the accuracy of ab initio quantum chemical calculations. Accurate modeling of the 2DIR spectra of solvated metal carbonyl complexes requires the development of new theoretical and computational tools beyond those employed in the standard analysis of one-dimensional IR spectra, and represents an ongoing challenge to currently available computational methodologies. These challenges are further compounded by the increasing interest in triggered 2DIR experiments that involve nonequilibrium vibrational dynamics on multiple electronic potential surfaces. In this Account, we review the various metal carbonyl complexes studied via 2DIR spectroscopy and outline the theoretical approaches used in order to model the spectra. The capabilities of 2DIR spectroscopy and its interplay with modern ab initio calculations are demonstrated in the context of the metal carbonyl complex Mn(2)(CO)(10) recently studied in our lab. Continued progress in experimental implementation and theoretical analysis will enable transient 2D spectroscopy to provide structurally sensitive details of complex, highly interacting nonequilibrium processes that are central to diverse chemical transformations.

Multilevel vibrational coherence transfer and wavepacket dynamics probed with multidimensional IR spectroscopy.

Multidimensional infrared (MDIR) spectroscopy of a strongly coupled multilevel vibrational system Mn(2)(CO)(10) (dimanganese decacarbonyl) in cyclohexane solution reveals fully resolved excited vibrational state coherences that exhibit slow 0.25-0.50 ps(-1) decay constants. Detailed analysis of the waiting-time dependence of certain cross-peak amplitudes shows modulation at multiple frequencies, providing a direct signature of excited vibrational coherences resulting from coherence transfer. A new signature of coherence transfer is observed as temporally modulated cross-peak amplitudes with more than one modulation frequency. The relative importance of different coherence transfer paths is considered in the context of the orientational response of a system which includes two vibrational modes with parallel dipole moments. Since MDIR spectroscopy enables spectral isolation of individual excited vibrational coherences (i.e., coherences between fundamental excitations), these experiments report directly on the frequency-frequency correlation functions of the excited states relative to each other as well as relative to the ground state. These results highlight the rich information contained in fully exploring three-dimensional third-order spectroscopy, particularly regarding chemically relevant slower dynamics and the importance of intramolecular interactions leading to dephasing by optically dark or low-frequency modes of the molecule.

Dissecting Enthalpic and Entropic Barriers to Ultrafast Equilibrium Isomerization of a Flexible Molecule Using 2DIR Chemical Exchange Spectroscopy

Ultrafast 2DIR chemical exchange spectroscopy was used to study the dynamic equilibrium between different isomers of dicobalt octacarbonyl. Exchange of population between bridged and unbridged isomers takes place on the time scale of a few picoseconds, corresponding to activation barriers of several kcal/mol. Despite overlapping spectral features in the 2DIR spectrum, the exchange component of the waiting time dependence was isolated by exploiting the well-characterized coherent modulation of nonexchange crosspeaks. The temperature dependence of the forward and reverse rate constants enabled extraction of isomerization energy barriers, where analysis using the Eyring equation indicated a substantial entropic contribution to the free energy barrier (DeltaS(double dagger)(exp) > 0). Comparison to quantum chemical calculations showed reasonable enthalpy agreement, but qualitative disagreement for the entropy of the transition state relative to the isomers (DeltaS(double dagger)(comp) < 0).

Watching solvent friction impede ultrafast barrier crossings: A direct test of Kramers theory

A systematic investigation of the solvents dynamic influence on activated barrier crossings on an electronic ground state is performed using ultrafast two-dimensional infrared chemical exchange spectroscopy. These measurements facilitate a direct comparison with the widely adopted Kramers theory of condensed phase reaction kinetics, and for the first time avoid the significant complication of electronic excitation to probe directly in the time domain a ground electronic state reaction with a well-defined transition state. The picosecond timescale interconversion between two stable isomers of the metal carbonyl complex Co(2)(CO)(8) in a series of linear alkane solvents shows negligible energetic variation with solvent carbon chain length, providing an exclusive probe of the effects of solvent friction. Relative to the linear alkane series, cyclohexane does alter the potential energy surface by preferentially stabilizing one of the isomers. Despite this pronounced modification of the reaction barrier energetics, combination of experiment and computation enables the removal of the nondynamical barrier contribution to the rate constant, isolating the dynamical influence of solvent friction. The experimental data, supported with quantum and classical computations, show agreement with a simple Markovian Kramers theory for the isomerization rate constants dependence on solvent viscosity.

Solvent-hindered intramolecular vibrational redistribution

Ultrafast two-dimensional infrared spectroscopy and molecular dynamics simulations of Mn(2)(CO)(10) in a series of linear alcohols reveal that the rate of intramolecular vibrational redistribution among the terminal carbonyl stretches is dictated by the average number of hydrogen bonds formed between the solute and solvent. The presence of hydrogen bonds was found to hinder vibrational redistribution between eigenstates, while leaving the overall T(1) relaxation rate unchanged.

Multiple Structures and Dynamics of [CpRu(CO)2]2 and [CpFe(CO)2]2 in Solution Revealed with Two-Dimensional Infrared Spectroscopy

Two-dimensional infrared (2DIR) spectroscopy is applied to both (Cp)(2)Fe(2)(CO)(4) and its ruthenium analog (Cp)(2)Ru(2)(CO)(4) in order to study the vibrational dynamics of these two systems. Combining the results of 2DIR spectroscopy and DFT calculations, the different structural forms of both the iron and the ruthenium complexes were characterized, furthering the previous assignment of the linear IR spectrum by determining the transition frequencies associated with the different isomeric forms. Monitoring the time-dependent amplitudes of the cross peaks enabled the observation of equilibrium energy transfer dynamics between different vibrational modes of the cis-B (Cp)(2)Fe(2)(CO)(4) and the gauche-NB (Cp)(2)Ru(2)(CO)(4) complexes. Treating the energy transfer as an equilibrium process, we extracted the rate constants associated with both the uphill and the downhill transfer of vibrational energy, finding that the difference in the rate constants of the two metal complexes maps to the difference in the energy gap between the two modes involved.

Energy transfer pathways in light-harvesting complexes of purple bacteria as revealed by global kinetic analysis of two-dimensional transient spectra.

Excited state dynamics in LH2 complexes of two purple bacterial species were studied by broad-band two-dimensional electronic spectroscopy. The optical response was measured in the 500-600 nm spectral region on the 0-400 fs time scale. Global target analysis of two-dimensional (2D) transient spectra revealed the main energy transfer pathways between carotenoid S2, 1Bu(-) and S1 states and bacteriochlorophyll Qx state. Global analysis ascertained the evolutionary and vibration-associated spectra, which also indicated the presence of a higher-lying vibrational level in the carotenoid S1 state. The estimation of the spectral overlap between the 1Bu(-) state and the Qx state indicated a significant contribution of the 1Bu(-) state to the overall S2-to-Qx excitation energy transfer.

Two-Dimensional Electronic Spectroscopy Reveals Ultrafast Downhill Energy Transfer in Photosystem I Trimers of the Cyanobacterium Thermosynechococcus elongatus.

Two-dimensional electronic spectroscopy (2DES) was used to investigate the ultrafast energy-transfer dynamics of trimeric photosystem I of the cyanobacterium Thermosynechococcus elongatus. We demonstrate the ability of 2DES to resolve dynamics in a large pigment-protein complex containing ∼300 chromophores with both high frequency and time resolution. Monitoring the waiting-time-dependent changes of the line shape of the inhomogeneously broadened Qy(0-0) transition, we directly observe downhill energy equilibration on the 50 fs time scale.

Ultrafast equilibrium and non-equilibrium chemical reaction dynamics probed with multidimensional infrared spectroscopy

Two-dimensional infrared (2D-IR) spectroscopy provides powerful tools to investigate chemical reaction dynamics in the condensed phase. Correlating excitation and detection frequencies grants access to structural and dynamical information that is hidden in a linear absorption spectrum. Low-barrier reactions naturally can occur on the picosecond time scale, and although they are too rapid to study using nuclear magnetic resonance spectroscopy, the intrinsic ultrafast time resolution of coherent 2D-IR spectroscopy enables direct tracking of equilibrium reactive barrier crossings. 2D-IR chemical exchange spectroscopy can monitor the picosecond dynamics of non-triggered chemical reactions by correlating excited reactant frequencies with detected product frequencies. Solvent and temperature-dependent variations enable comparisons with microscopic rate theories at an unprecedented level of detail. 2D-IR spectroscopy is also emerging as a powerful probe of non-equilibrium light-driven chemical transformations. Transient 2D-IR spectroscopy is able to follow nascent photoproducts caused by electronic excitation or by a temperature jump. Soon it will be possible to study transient species with the full range of 2D observables, such as line shapes and waiting-time dynamics that have motivated the wide adoption of equilibrium 2D-IR spectroscopy. This review summarises the general progress in using 2D-IR spectroscopy to study chemical reactions in solution, focusing on our investigations into reactions of isomerisation of CO2(CO)8, photodissociation of Mn2(CO)10, geminate rebinding in [CpMo(CO)3]2 and charge transfer in betaine-30 as viewed from the first solvation shell.