Molecular dynamics simulations of cooling in laser-excited heme proteins.

Abstract

In transient optical experiments the absorbed photon raises the vibrational temperature of the chromophore. In heme proteins at room temperature conversion of a 530-nm photon into vibrational energy is estimated to raise the temperature of the heme by 500-700 K. Cooling of the heme is expected to occur mainly by interacting with the surrounding protein. We report molecular dynamics simulations for myoglobin and cytochrome c in vacuo that predict that this cooling occurs on the ps time scale. The decay of the vibrational temperature is nonexponential with about 50% loss occurring in 1-4 ps and with the remainder in 20-40 ps. These results predict the presence of nonequilibrium vibrational populations that would introduce ambiguity into the interpretation of transient ps absorption and Raman spectra and influence the kinetics of sub-ns geminate recombination.slowly than the time resolution of conventional ps laser experiments (12-15). There is, therefore, a reasonable expectation that the heme group in the protein will retain vibrational energy in excess of equilibrium for measurably long times following optical excitation.If one or more photons of wavelength X were absorbed by a heme group that was initially at equilibrium at 300 K with average vibrational energy (E) exclusive of zero-point energy and if the excitation were distributed by the intramolecular vibrational relaxation over all the harmonic vibrational modes of the ground electronic state in accordance with Boltzmann statistics, the new molecular temperature T would be obtained by satisfying the relationAfter molecules absorb visible or ultraviolet light, the deposited energy becomes distributed over a subset of the molecular motions and subsequently is exchanged with the surroundings. When ps or fs light pulses are used to probe photophysical or photochemical processes, it is necessary to consider that nonequilibrium distributions of vibrational energy may persist during the time scale of the experiment. Transient excesses of vibrational energy can alter the rates of chemical and physical transformations, and they may also introduce spectral changes that could easily be mistaken for chemical steps in a process.Transient spectra of heme proteins have been studied with ps (1-7) and fs (8, 9) time resolution in experiments that have exposed a variety of spectral intermediates following light absorption by the heme group. The principal goal of such experiments is to understand the sequence of early structural alterations occurring after a diatomic ligand (02, CO, NO) is photodissociated from the heme iron. On these time scales the photolyzed sample may also contain electronically excited states, each of which may have a spectrum that changes with time as a result of changes in its vibrational energy content. The present paper is an attempt to predict, on the basis of molecular dynamics simulations, the rate at which the excess vibrational energy in the heme is dissipated into the protein.To understand the detailed pathways for vibrational cooling ...

Heat transfer in protein–water interfaces

“…This is of the order of 10-20 ps for the proteins investigated in this work. We have fitted the simulated temperature relaxation data to equation (6) to quantify the thermal diffusivity, thermal conductivity and the thermal conductance of the protein-water interface. Table 2 contains numerical data of the heat transport properties of the proteins for (T i ,T s )=(350,250) K. To test the sensitivity of our results to the simulation conditions we performed simulations with different initial and solvent temperatures, (400,300) K and (350,250) K. We obtained the same results within the statistical accuracy of our method.…”

“…5 Chemical and photochemical reactions occurring at specific spots in biomolecules can result in large increases in temperature in very small volumes. Transient photon experiments, where photon absorption is converted to vibrational energy, show that the temperature rise resulting from this process can be very significant, between 500 and 1000 K. 6,7 Recent work on the Ca 2+ -ATPase embedded in the sarcoplasmic reticulum has suggested that this enzyme can -under working conditions -release significant amounts of heat. Using micro-thermometers it was found that thermal gradients of the order of 10 5 K/m can develop between regions separated by tens of micrometers.…”

“…The first simulation study of vibrational energy relaxation of heme proteins was reported in reference. 6 These simulations relied on the injection of vibrational energy by an amount equivalent to the energy associated to photon absorption. Subsequent methodologies have exploited the scaling of the energy diffusion coefficient with the vibrational mode frequency of a protein, 10 or have modelled the heat transfer process as a boundary thermal transport problem.…”

Vibrational Dynamics of Carbon Monoxide at the Active Site of Myoglobin: Picosecond Infrared Free-Electron Laser Pump-Probe Experiments

“…30 CO vibrational relaxation can be investigated using the techniques of molecular dynamics 31,32 because VR occurs on a suitable (sub-nanosecond) time scale. In contrast to simulations of picosecond time scale photoinduced processes in Mb such as photodissociation 33,34 or vibrational cooling, 35 carbonyl VR occurs solely on the ground electronic potential surface, and simulations need not invoke ad hoc assumptions about the nature of heme electronic transitions. The VR of excited CO can also be studied by exact quantum dynamics calculations, which are presently capable of modeling the shorttime behavior of a diatomic molecule weakly coupled to harmonic baths of arbitrary complexity.…”

Investigations of Coherent Vibrational Oscillations in Myoglobin

“…The relaxation dynamics of this nonequilibrium structure toward equilibrium has been extensively studied over broad time scales using a variety of techniques. [26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41][42][43] In this work, we tune the laser carrier frequency into resonance with the strong Soret absorption band of myoglobin near 420-435 nm in order to both pump and probe the various sample states. This allows us to selectively probe the dynamics of the active site (heme) and its interaction with the protein.…”