Thermal boundary conductance at the myoglobin–water interface: Heme cooling mechanism in light and heavy water environments

The molecular mechanism of heme cooling following the photoexcitation of heme proteins has been a central issue in biological chemical physics for several decades. We expect that such a non-equilibrium process is accompanied by a vibrational energy relaxation from one site (protein quake epicenter) to the other sites in the protein molecule and eventually to the solvent molecules surrounding the protein. Interestingly, a recent optical-pump THz-probe spectroscopy demonstrated that the energy dissipation rate from the photoexcited heme of myoglobin in the D2O environment was slower than that in H2O, the mechanism of which remains unclear. To address the issue, we investigated the energy dissipation mechanism at the myoglobin-water interface with a special emphasis on the roles of the heme propionate side chains. After performing the equilibrium molecular dynamics simulation of myoglobin in both D2O and H2O environments, we calculated the vibrational density of states, from which we evaluated the solvent substitution effect on the heme side chain dynamics. In addition, the structure of the solvation shell around each heme side chain was examined using the radial distribution function of waters. Furthermore, we estimated the thermal boundary conductance at the myoglobin-water interface and discussed the heme cooling mechanism by exploiting a thermal RC circuit model for the protein-water interface. The calculated value of the thermal boundary conductance of the myoglobin-water interface was larger in H2O than that in D2O, in line with the experimental observation. Furthermore, we estimated the thermal relaxation time at the myoglobin-water interface based on the thermal RC circuit model.