The Orange Carotenoid Protein (OCP) is a photoactive protein involved in photoprotection of Cyanobacteria. Recently, a photoactivation mechanism was proposed for OCP, in which the initially excited S2 state yields multiple ps-lived excited states (ICT, S1, S*), but structural evidence is missing. Importantly, only one of these leads to the biologically active OCP-red state on the second timescale. We propose to conduct an ultra-fast time-resolved crystallography experiment at an X-ray free electron laser (XFEL) on OCP to accurately characterize the structures of the short-lived photo-intermediates on the femtosecond to millisecond timescale. In parallel, we will use the new time-resolved crystallography beamline of the ESRF to determine the structures of the later intermediates forming on the millisecond to second timescale. By allowing to visualize protein conformational changes upon photoactivation from the photochemical (hundreds of femtoseconds) to the photobiological timescales (seconds), our integrated structural biology project will allow to (i) test mechanistic hypotheses, (ii) pave the way to a detailed understanding the photophysical properties of OCP, and (iii) open avenues towards its exploitation as an optogenetic component or a regulator of light-uptake in biomimetic photosynthetic systems.