The function of photoreceptors relies on efficient transfer of absorbed light energy from the chromophore to the protein in order to drive conformational changes that ultimately generate an output signal. In retinal binding proteins, mainly two mechanisms exist to store the photon energy after photoisomerization: (1) conformational distortion of the prosthetic group retinal, and (2) charge separation between the protonated retinal Schiff base (RSBH+) and its counter-ion complex. Accordingly, energy transfer to the protein is achieved by chromophore relaxation and/ or reduction of the charge separation in the RSBH+-counter-ion complex. Combining FTIR and UV-Vis spectroscopy along with molecular dynamics simulations, we show here for the widely used red-activatable Volvox carteri channelrhodopsin-1 derivate ReaChR that energy storage and transfer into the protein depends on the protonation state of glutamic acid E163 (Ci1), one of the counter-ions of the RSBH+. Ci1 retains a pKa of 7.6, so that both its protonated and deprotonated forms equilibrate at physiological conditions. Protonation of Ci1 leads to a rigid hydrogen-bonding network in the active-site region. This stabilizes the distorted conformation of the retinal after photoactivation and decelerates energy transfer into the protein by impairing release of the strain energy. In contrast, with deprotonated Ci1 or removal of the Ci1 glutamate side chain, the hydrogen-bonded system is less rigid and energy transfer by chromophore relaxation is accelerated. Based on the hydrogen out-of-plane (HOOP) band decay kinetics, we determined the activation energy for these processes in dependence of the Ci1 protonation state.