The Orange Carotenoid Protein (OCP), involved in energy-quenching of the cyanobacterial light-harvesting antennae, is a two-domain protein functionalized by a non-covalently bound keto-carotenoid. To elicit its photoprotection function, the protein must be photoactivated by a blue-green photon, triggering transition from an orange inactive “dark” state (OCPO) to a red photoactive “light” state (OCPR). The photoactivation mechanism, which spans 13 decades in time, involves structural rearrangements at the level of both the photoexcited carotenoid and the protein scaffold. During my thesis, I investigated rhe OCP photoactivation mechanism using variety of biochemistry and structural biology methods. Firstly, through combination of spectroscopy and steady-state and time-resolved (TR) X-ray cattering, we examined the large-scale motions involved in the photoactivation and recovery of OCP. We demonstrated that oligomerization occurs at both the OCPO and OCPR level, and that it partakes in the regulation of the protein photoactivation and thermal recovery. Secondly, by using conventional X-ray crystallography, we determined the previously-uncharacterized crystal structure of Planktothrix aghardii OCP. Structural analysis pointed to the influence of protein flexibility on the photoactivation and recovery rates, and on the energy-quenching activity of this variant. In an effort to characterize early stages of OCP photoactivation by means of TR crystallography, we investigated in vitro and in vivo crystallization methods to produce submicron-sized OCP crystals. Specifically, we attempted in vivo crystallization in the crystalliferous bacterium Bacillus thuringiensis (Bt), endeavoring to obtain crystals of fusions of OCP with Cyt1Aa and Cry11Aa Bt toxins. While unsuccessful in terms of production of OCP crystals, this work enabled to shed light on the structure and bioactivation cascade of the two toxins, and to investigate the molecular mechanisms at the basis of their crystallization.