Adaptation to rapid environmental changes is crucial for maintaining optimal photosynthetic efficiency and is ultimately key to the survival of all photosynthetic organisms. In cyanobacteria, the major aquatic primary producers, photoregulation is controlled by the orange carotenoid protein (OCP) photocycle. OCP is the only known photoreceptor that uses a carotenoid for light activation. Understanding and potentially controlling this unique photocycle could open up new opportunities for optogenetics and improving photosynthetic biomass. How the carotenoid drives and controls it remains unclear. It has long been argued that OCP photoactivation is initiated in the C-terminal domain (CTD) by H-bond cleavage between the carbonyl group of the carotenoid β1-ring and adjacent residues. However, my recent crystallographic results suggest that the H-bond cleavage occurs after carotenoid isomerisation and rearrangement of the N-terminal domain (NTD) (ref 1). All this suggests that previous models of the OCP photocycle should be re-evaluated. To better understand the role of the NTD in the photocycle, we have performed temperature-dependent spectroscopy, flash photolysis and pump-probe transient absorption on the two OCP forms: Canthaxanthin-bound OCP (OCPCAN) and Echinenone-bound OCP (OCPECH). The difference between the two carotenoids is the presence of a carbonyl group in the β2-ring located in the NTD of the protein. The applied spectroscopic approach allowed us to report the previously unresolved OCP intermediate, mainly associated with the absorption bleach. We show that the steps of the OCP photocycle are always faster in OCPCAN than in OCPECH: from 2 to almost 20 times, depending on the step. These results suggest that the presence of the carbonyl group in the β2-ring of the carotenoid accelerates the OCP photocycle and that NTD plays an important role in the OCP photocycle, at least in the μs-s time range. An updated model of the OCP photocycle is proposed.