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

Westlake, Brittany C.; Brennaman, M. Kyle; Concepcion, Javier J.; Paul, Jared J.; Bettis, Stephanie E.; Hampton, Shaun; Miller, Stephen A.; Лебедева, Н. В.; Forbes, Malcolm D. E.; Moran, Andrew M.; Meyer, Thomas J.; Papanikolas, John M.

doi:10.1073/pnas.1104811108

Cited by 97 publications

(172 citation statements)

References 16 publications

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“…A charge rearrangement occurs upon photoexcitation such that electron density is transferred from the acidic functional group, often a hydroxyl group, to the aromatic ring (40,41). Photoacidic coumarins have been used in previous studies to mimic electron and proton transfer reactions in solution (41,42) and in the active site of KSI (31).…”

Section: Resultsmentioning

confidence: 99%

Direct measurement of the protein response to an electrostatic perturbation that mimics the catalytic cycle in ketosteroid isomerase

Jha¹,

Gaffney

et al. 2011

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

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Understanding how electric fields and their fluctuations in the active site of enzymes affect efficient catalysis represents a critical objective of biochemical research. We have directly measured the dynamics of the electric field in the active site of a highly proficient enzyme, Δ 5 -3-ketosteroid isomerase (KSI), in response to a sudden electrostatic perturbation that simulates the charge displacement that occurs along the KSI catalytic reaction coordinate. Photoexcitation of a fluorescent analog (coumarin 183) of the reaction intermediate mimics the change in charge distribution that occurs between the reactant and intermediate state in the steroid substrate of KSI. We measured the electrostatic response and angular dynamics of four probe dipoles in the enzyme active site by monitoring the time-resolved changes in the vibrational absorbance (IR) spectrum of a spectator thiocyanate moiety (a quantitative sensor of changes in electric field) placed at four different locations in and around the active site, using polarization-dependent transient vibrational Stark spectroscopy. The four different dipoles in the active site remain immobile and do not align to the changes in the substrate electric field. These results indicate that the active site of KSI is preorganized with respect to functionally relevant changes in electric fields.enzyme catalysis | electrostatic preorganization | Stark effect | visible-pump IR probe | time-resolved anisotropy E nzymes catalyze the vast majority of biochemical reactions and accelerate the rate of these reactions by many orders of magnitude compared to the uncatalyzed reactions in solution. The origins of the enormous catalytic power of enzymes are still not well understood despite enormous effort (1-6). In particular, the functional role of fast picosecond protein motions in catalysis and the dynamic nature of the transition state barrier crossing is a subject of ongoing and current debate (7-13). Theoretical studies have suggested that fast vibrations in enzymes might generate transition state conformations conducive to the chemical reaction (7,8,(14)(15)(16)(17)(18)(19)(20)(21), a familiar concept for reactions in ordinary solvents (22). In an alternative viewpoint, preorganization effects have been suggested to be a major contributing factor to enzyme catalysis (23-28). It has been postulated that enzymes have partially oriented dipoles of polar and charged groups in the active site that interact with electrostatic features present in the catalytic transition state more favorably than water can. Such preorganization of active site dipoles and charges has been suggested to result in a reduction in the reorganization energy and provide enormous catalytic advantage over the reaction in solution, where water molecules must rearrange in order to solvate charge rearrangements during the chemical reaction (24,(29)(30)(31). The relative merits of these opposing viewpoints remains unclear largely because of the paucity of direct experimental assessment of the key discrepancies betwee...

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Section: Resultsmentioning

confidence: 99%

Direct measurement of the protein response to an electrostatic perturbation that mimics the catalytic cycle in ketosteroid isomerase

Jha¹,

Gaffney

et al. 2011

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

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“…The resulting oxidation of the Bi-PhOH unit dramatically enhances the acidity of the phenolic proton (Δ pKa ∼ 12) (25,26), which creates the chemical potential required for proton transfer to the hydrogen-bonded benzimidazole moiety (27)(28)(29)(30). Therefore, excitation of triad 1 is expected to lead to eventual formation of a charge-separated state characterized by cationic benzimidazole, a phenoxyl radical, a neutral PF 10 , and a reduced TCNP porphyrin (BiH þ -PhO • -PF 10 -TCNP •− ).…”

Section: Resultsmentioning

confidence: 99%

Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation

Megiatto

Antoniuk-Pablant

Sherman

et al. 2012

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

111

112

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In the photosynthetic photosystem II, electrons are transferred from the manganese-containing oxygen evolving complex (OEC) to the oxidized primary electron-donor chlorophyll P680 •+ by a proton-coupled electron transfer process involving a tyrosine-histidine pair. Proton transfer from the tyrosine phenolic group to a histidine nitrogen positions the redox potential of the tyrosine between those of P680 •+ and the OEC. We report the synthesis and time-resolved spectroscopic study of a molecular triad that models this electron transfer. The triad consists of a high-potential porphyrin bearing two pentafluorophenyl groups (PF 10 ), a tetracyanoporphyrin electron acceptor (TCNP), and a benzimidazole-phenol secondary electron-donor (Bi-PhOH). Excitation of PF 10 in benzonitrile is followed by singlet energy transfer to TCNP ( τ = 41 ps), whose excited state decays by photoinduced electron transfer ( τ = 830 ps) to yield . A second electron transfer reaction follows ( τ < 12 ps), giving a final state postulated as BiH + -PhO • -PF 10 -TCNP •- , in which the phenolic proton now resides on benzimidazole. This final state decays with a time constant of 3.8 μs. The triad thus functionally mimics the electron transfers involving the tyrosine-histidine pair in PSII. The final charge-separated state is thermodynamically capable of water oxidation, and its long lifetime suggests the possibility of coupling systems such as this system to water oxidation catalysts for use in artificial photosynthetic fuel production.

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“…Such observations are incompatible with the tunneling mechanism advanced to explain O-H bond fission in the gas phase or in cyclohexane but could be explained by near-threshold autoionization from the PhOH(S 1 ) origin to the PhOH + (aq) + e -(aq) asymptote followed by rapid deprotonation 105 or, possibly, in terms of an excited state proton-coupled electron transfer process. 106,107 Summarising, there is a growing body of evidence to support the thesis that the fragmentation dynamics established from careful gas-phase studies can provide valuable insights into the early stages of the photodissociation of that same solute in a weakly interacting solvent. This is tantamount to saying that, in such cases, the underlying PESs and the non-adiabatic couplings that govern the dissociation of the isolated molecule are not substantially perturbed when the molecule is in the presence of a weakly interacting solvent.…”

Section: 100mentioning

confidence: 99%

Molecular Photofragmentation Dynamics in the Gas and Condensed Phases

Ashfold

Murdock

Oliver

2017

Annu. Rev. Phys. Chem.

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This is the submitted manuscript. The final published version (version of record) is available online via Annual Review of Physical Chemistry at http://www.annualreviews.org/doi/10.1146/annurev-physchem-052516-050756 . Please refer to any applicable terms of use of the publisher University of Bristol -Explore Bristol Research General rightsThis document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/pure/about/ebr-terms 1 Molecular Photofragmentation Dynamics in the Gas and Condensed PhasesMichael N.R. Ashfold, Daniel Murdock and Thomas A.A. Oliver School of Chemistry, University of Bristol, Bristol, U.K., BS8 1TS AbstractExciting a molecule with a UV photon often leads to bond fission, but the final outcome of the bond cleavage is typically both molecule and phase dependent. The photodissociation of an isolated gasphase molecule can be viewed as closed system: energy and momentum are conserved, and the fragmentation is irreversible. The same is not true in a solution-phase photodissociation process.Solvent interactions may dissipate some of the photoexcitation energy prior to bond fission, and will dissipate any excess energy partitioned into the dissociation products. Products that have no analogue in the corresponding gas-phase study may arise by, for example, geminate recombination. Here we illustrate the extents to which dynamical insights from gas-phase studies can inform our understanding of the corresponding solution-phase photochemistry and how, in the specific case of photoinduced ring-opening reactions, solution-phase studies can in some cases reveal dynamical insights more clearly than the corresponding gas-phase study.Keywords photochemistry, photodissociation, photoinduced ring opening, non-adiabatic dynamics, conical intersections. 2 HISTORICAL CONTEXTCiamician is recognised as a pioneer of (organic) photochemistry and an early advocate for fuel production by means of artificial photo'synthesis'. 1 His studies were performed in solution and usually driven by sunlight, at a time when the concept of the photon was yet to be fully accepted.Identifying the ultimate reaction products was in itself a major achievement, and any ideas regarding reaction mechanism were rudimentary. Even the concatenation of ideas like ground and excited electronic states, radiative and non-radiative transitions, spin multiplicity, etc, into what would later be termed a Jablonski diagram 2 still lay far in the future.A potentially more fruitful path at that time for those curious about the mechanisms of photochemical reactions was to focus on very simple molecular systems -diatomic and 'diatomic-like' molecules. generally polychromatic) light sources were now available, and the development of grating spectrometers enabled the recording of electronic absorption spectra for many small gas-phase molecules. Vibrational and even rotational fine structure was resolved and interpreted in many such ...

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

Cited by 97 publications

References 16 publications

Direct measurement of the protein response to an electrostatic perturbation that mimics the catalytic cycle in ketosteroid isomerase

Direct measurement of the protein response to an electrostatic perturbation that mimics the catalytic cycle in ketosteroid isomerase

Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation

Molecular Photofragmentation Dynamics in the Gas and Condensed Phases

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