Article

Photoactivation of the photoactive yellow protein: Why photon absorption triggers a trans-to-cis lsomerization of the chromophore in the protein

Università degli Studi di Siena, Siena, Tuscany, Italy
Journal of the American Chemical Society (Impact Factor: 11.44). 05/2004; 126(13):4228-33. DOI: 10.1021/ja039557f
Source: PubMed

ABSTRACT Atomistic QM/MM simulations have been carried out on the complete photocycle of Photoactive Yellow Protein, a bacterial photoreceptor, in which blue light triggers isomerization of a covalently bound chromophore. The "chemical role" of the protein cavity in the control of the photoisomerization step has been elucidated. Isomerization is facilitated due to preferential electrostatic stabilization of the chromophore's excited state by the guanidium group of Arg52, located just above the negatively charged chromophore ring. In vacuo isomerization does not occur. Isomerization of the double bond is enhanced relative to isomerization of a single bond due to the steric interactions between the phenyl ring of the chromophore and the side chains of Arg52 and Phe62. In the isomerized configuration (ground-state cis), a proton transfer from Glu46 to the chromophore is far more probable than in the initial configuration (ground-state trans). It is this proton transfer that initiates the conformational changes within the protein, which are believed to lead to signaling.

0 Followers
 · 
145 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: In light-driven single-molecule rotary motors, the photoisomerization of a double bond converts light energy into the rotation of a moiety (the rotor) with respect to another (the stator). However, at the level of a molecular population, an effective rotary motion can only be achieved if a large majority of the rotors rotate in the same, specific direction. Here we present a quantitative investigation of the directionality (clockwise vs counterclockwise) induced by a single stereogenic center placed in allylic position with respect to the reactive double bond of a model of the biomimetic indanylidene-pyrrolinium framework. By computing ensembles of nonadiabatic trajectories at 300 K, we predict that the photoisomerization is >70% unidirectional for the Z → E and E → Z conversions. Most importantly, we show that such directionality, resulting from the asymmetry of the excited state force field, can still be observed in the presence of a small (ca. 2°) pretwist or helicity of the reactive double bond. This questions the validity of the conjecture that a significant double-bond pretwist (e.g., >10°) in the ground state equilibrium structure of synthetic or natural rotary motors would be required for unidirectional motion.Keywords: photochemistry; isomerization; molecular motor; ab initio nonadiabatic molecular dynamics
    Journal of Physical Chemistry Letters 01/2015; 6(4):599-604. DOI:10.1021/jz502644h · 6.69 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Serial femtosecond crystallography using ultrashort pulses from x-ray free electron lasers (XFELs) enables studies of the light-triggered dynamics of biomolecules. We used microcrystals of photoactive yellow protein (a bacterial blue light photoreceptor) as a model system and obtained high-resolution, time-resolved difference electron density maps of excellent quality with strong features; these allowed the determination of structures of reaction intermediates to a resolution of 1.6 angstroms. Our results open the way to the study of reversible and nonreversible biological reactions on time scales as short as femtoseconds under conditions that maximize the extent of reaction initiation throughout the crystal.
    Science 12/2014; 346(6214):1242-1246. DOI:10.1126/science.1259357 · 31.48 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Accurate predictions of photoexcitation properties are a major challenge for modern methods of theoretical chemistry. We show here how approximate coupled-cluster singles and doubles (CC2) calculations in combination with the reduced virtual space (RVS) approach can be employed in studies of excited states of large biomolecular systems. The RVS-CC2 approach is used for accurately predicting optical properties of the p-hydroxybenzylidene-dihydroimidazolinone (p-HBDI) chromophore embedded in green fluorescent protein (GFP) models using quantum mechanical calculations in combination with large basis sets. We study the lowest excited states for the isolated and protein-embedded chromophore in two different protonation states, and show how omitting high-lying virtual orbitals in the RVS calculation of excitation energies renders large-scale CC2 studies computationally feasible. We also discuss how the error introduced by the RVS approach can be systematically estimated and controlled. The obtained CC2 excitation energies of 3.13-3.27 eV and 2.69-2.77 eV for the two protonation states of different protein models are in excellent agreement with the maxima of the experimental absorption spectra of 3.12-3.14 eV and 2.61-2.64 eV, respectively. Thus, the calculated energy splitting between the excited states of the two protonation states is 0.44-0.52 eV, which agrees very well with the experimental value of 0.48-0.51 eV. The calculations at the RVS-CC2 level on the protein models show the importance of using large QM regions in studies of biochromophores embedded in proteins.
    The Journal of Physical Chemistry B 01/2015; 119(7). DOI:10.1021/jp5120898 · 3.38 Impact Factor

Preview

Download
0 Downloads
Available from