Local vibrational coherences drive the primary photochemistry of vision

Johnson, Philip J. M.; Halpin, Alexei; Morizumi, Takefumi; Prokhorenko, Valentyn I.; Ernst, Oliver P.; Miller, R. J. Dwayne

doi:10.1038/nchem.2398

Cited by 178 publications

(255 citation statements)

References 58 publications

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“…The present analysis thus assumes that the ensemble phase relation resulting from the optical pulse is maintained in this description up to the transition time. This does however not constitute evidence for a coherent reaction coordinate, such as seen on considerably faster timescale in photoisomerisation of rhodopsin from transient grating spectroscopy [28]. Future experimental investigations may revisit this observation in PYP, applying for example multi-pulse pumpdump-probe experiments.…”

Section: Primary Photochemical Reactions and Coherence Of Pypmentioning

confidence: 99%

Populations and coherence in femtosecond time resolved X-ray crystallography of the photoactive yellow protein

Hutchison

Thor

2017

International Reviews in Physical Chemistry

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Ultrafast X-ray crystallography of the Photoactive Yellow Protein with femtosecond delays using an X-ray Free Electron Laser has successfully probed the dynamics of an early FranckCondon species. The femtosecond pump-probe application of protein crystallography represents a new experimental regime that provides an X-ray structural probe for coherent processes that were previously accessible primarily using ultrafast spectroscopy. We address how the optical regime of the visible pump, that is necessary to successfully resolve ultrafast structural differences, affects the motions that are measured using the technique. The subpicosecond photochemical dynamics in PYP involves evolution of a mixture of electronic ground and excited state populations. Additionally, within the dephasing time structural motion include vibrational coherence arising from excited states, the ground state and a ground state intermediate under experimental conditions used for ultrafast crystallography. Intense optical pulses are required to convert population levels in PYP crystals that allow detection by X-ray crystallography, but the compromise currently needed for the optical bandwidth and power has consequences with regard to the contributions to the motions that are experimentally measured with femtosecond delays. We briefly review the ultrafast spectroscopy literature of the primary photoreactions of PYP and discuss relevant physical models taken from coherent control and femtosecond coherence spectroscopy literature that address both the population transfer as well 2 as the vibrational coherences. We apply linear response theory, with the additional use of a high power approximation, of on-resonance impulsive vibrational coherence in the ground state and the non-impulsive coherence in the excited state and discuss experimental approaches to manipulate the coherence contributions. The results are generalised and extended to discuss the future capabilities of high repetition rate XFEL instruments providing enhanced sensitivity to perform the crystallographic equivalent of an impulsive Raman measurement of vibrational coherence.

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Section: Primary Photochemical Reactions and Coherence Of Pypmentioning

confidence: 99%

Populations and coherence in femtosecond time resolved X-ray crystallography of the photoactive yellow protein

Hutchison

Thor

2017

International Reviews in Physical Chemistry

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Section: Main Textmentioning

confidence: 99%

“…Indeed, nuclear and electronic wave functions often strongly interact with each other, leading to exotic phenomena whereby vibrational motion can mediate and dictate the rate and efficiency of electronic transitions. [2][3][4][5] With overwhelming evidence that nuclear-electronic (vibronic) interactions play a crucial role in a broad range of systems, including light harvesting and conversion in photosynthetic organisms, 6-11 this phenomenon represents a tremendous opportunity to acquire deeper knowledge and control over the structural traits that govern molecular function and reactivity.Recent efforts led by Rubtsov et al,12,13 Bakulin et al, 14 and our group 15,16 have shown that one way to experimentally exploit vibronic coupling to modulate molecular function is to introduce targeted vibrational excitation along specific reaction co-ordinates using ultrafast mid-infrared (IR) pulses. This approach enables promoting or suppressing electronic transitions, notably photo-induced electron transfer (ET), an elementary process that pervades the natural world.…”

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confidence: 99%

Directing the path of light-induced electron transfer at a molecular fork using vibrational excitation

et al. 2017

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Ultrafast electron transfer in condensed-phase molecular systems is often strongly coupled to intramolecular vibrations that can promote, suppress and direct electronic processes. Recent experiments exploring this phenomenon proved that light-induced electron transfer can be strongly modulated by vibrational excitation, suggesting a new avenue for active control over molecular function. Here, we achieve the first example of such explicit vibrational control through judicious design of a Pt(II)-acetylide charge-transfer Donor-Bridge-Acceptor-Bridge-Donor "fork" system: asymmetric 13 C isotopic labelling of one of the two -C≡C-bridges makes the two parallel and otherwise identical Donor→Acceptor electron-transfer pathways structurally distinct, enabling independent vibrational perturbation of either. Applying an ultrafast UV pump (excitation)-IR pump (perturbation)-IR probe (monitoring) pulse sequence, we show that the pathway that is vibrationally perturbed during UV-induced electron-transfer is dramatically slowed down compared to its unperturbed counterpart. One can thus choose the dominant electron transfer pathway. The findings deliver a new opportunity for precise perturbative control of electronic energy propagation in molecular devices. Main TextControlling the function of future advanced materials demands a profound understanding of energymatter interactions in molecular systems at the quantum level. 1 There is a growing consensus that energy-and electron-transfer processes occurring far away from equilibrium in condensed-phase systems on femto-to-picosecond timescales do not conform to the Born-Oppenheimer approximation. Indeed, nuclear and electronic wave functions often strongly interact with each other, leading to exotic phenomena whereby vibrational motion can mediate and dictate the rate and efficiency of electronic transitions. [2][3][4][5] With overwhelming evidence that nuclear-electronic (vibronic) interactions play a crucial role in a broad range of systems, including light harvesting and conversion in photosynthetic organisms, 6-11 this phenomenon represents a tremendous opportunity to acquire deeper knowledge and control over the structural traits that govern molecular function and reactivity.Recent efforts led by Rubtsov et al.,12,13 Bakulin et al., 14 and our group 15,16 have shown that one way to experimentally exploit vibronic coupling to modulate molecular function is to introduce targeted vibrational excitation along specific reaction co-ordinates using ultrafast mid-infrared (IR) pulses. This approach enables promoting or suppressing electronic transitions, notably photo-induced electron transfer (ET), an elementary process that pervades the natural world. Although the demonstrated excited state modulations have been remarkably efficient, up to 100% suppression in one case, 15 predictive and directive control of electron transfer in the condensed phase has not been achieved yet.

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“…Rhodopsin (RH1) has been extensively characterized across vertebrates, with studies largely focused on how its spectral properties (i.e., wavelength of maximum absorbance, λ MAX ) can be linked to adaptation to various spectral environments (12,13). Beyond spectral tuning, recent in vitro work has also highlighted the importance of the kinetics of activation and stability of rhodopsin (14)(15)(16), aspects of the proteins function that are considered evolutionary innovations for dim-light vision and are likely similarly critical for proper receptor functioning and organismal fitness (17)(18)(19)(20)(21). These important functional properties are modulated by amino acid sites distributed across the protein structure (22)(23)(24)(25); however, several are located near conserved GPCR elements maintaining stability (26)(27)(28), such as the intramolecular HBN (29)(30)(31)(32).…”

mentioning

confidence: 99%

Evolution of nonspectral rhodopsin function at high altitudes

Castiglione

Hauser

Liao

et al. 2017

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

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High-altitude environments present a range of biochemical and physiological challenges for organisms through decreases in oxygen, pressure, and temperature relative to lowland habitats. Proteinlevel adaptations to hypoxic high-altitude conditions have been identified in multiple terrestrial endotherms; however, comparable adaptations in aquatic ectotherms, such as fishes, have not been as extensively characterized. In enzyme proteins, cold adaptation is attained through functional trade-offs between stability and activity, often mediated by substitutions outside the active site. Little is known whether signaling proteins [e.g., G protein-coupled receptors (GPCRs)] exhibit natural variation in response to cold temperatures. Rhodopsin (RH1), the temperature-sensitive visual pigment mediating dim-light vision, offers an opportunity to enhance our understanding of thermal adaptation in a model GPCR. Here, we investigate the evolution of rhodopsin function in an Andean mountain catfish system spanning a range of elevations. Using molecular evolutionary analyses and site-directed mutagenesis experiments, we provide evidence for cold adaptation in RH1. We find that unique amino acid substitutions occur at sites under positive selection in high-altitude catfishes, located at opposite ends of the RH1 intramolecular hydrogen-bonding network. Natural high-altitude variants introduced into these sites via mutagenesis have limited effects on spectral tuning, yet decrease the stability of dark-state and light-activated rhodopsin, accelerating the decay of ligand-bound forms. As found in cold-adapted enzymes, this phenotype likely compensates for a cold-induced decrease in kinetic rates-properties of rhodopsin that mediate rod sensitivity and visual performance. Our results support a role for natural variation in enhancing the performance of GPCRs in response to cold temperatures.H igh-altitude environments impose a suite of biochemical and physiological constraints on organisms, such as hypoxia, low atmospheric pressure, and decreasing temperatures (1-3). At the biochemical level, proteins adapted to such conditions are of particular interest to evolutionary biologists (1, 4). Studies of high-altitude-adapted organisms, especially endotherms, have focused primarily on adaptation to hypoxia, including modification of proteins involved in oxygen metabolism (2, 5), and hemoglobin structure and function (6). In contrast, our understanding of biochemical adaptations for high altitude in ectothermic organisms, for which cold temperatures impose unique constraints (7-9), remains limited. Studies in prokaryotes have highlighted how cold adaptation in enzymes is attained by functional trade-offs between protein stability and activity (10), a trade-off also characterized in enzymes from ectothermic vertebrates, such as teleost fishes, where single mutations altering intramolecular hydrogen bonding networks (HBNs) decrease protein stability and ligand binding affinity to optimize kinetic rates for cold environments (11). It is currently...

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Local vibrational coherences drive the primary photochemistry of vision

Cited by 178 publications

References 58 publications

Populations and coherence in femtosecond time resolved X-ray crystallography of the photoactive yellow protein

Populations and coherence in femtosecond time resolved X-ray crystallography of the photoactive yellow protein

Directing the path of light-induced electron transfer at a molecular fork using vibrational excitation

Evolution of nonspectral rhodopsin function at high altitudes

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