Plants, algae, and cyanobacteria have developed mechanisms to decrease the energy arriving at reaction centers to protect themselves from high irradiance. In cyanobacteria, the photoactive Orange Carotenoid Protein (OCP) and the Fluorescence Recovery Protein are essential elements in this mechanism. Absorption of strong blue-green light by the OCP induces carotenoid and protein conformational changes converting the orange (inactive) OCP into a red (active) OCP. Only the red orange carotenoid protein (OCP r ) is able to bind to phycobilisomes, the cyanobacterial antenna, and to quench excess energy. In this work, we have constructed and characterized several OCP mutants and focused on the role of the OCP N-terminal arm in photoactivation and excitation energy dissipation. The N-terminal arm largely stabilizes the closed orange OCP structure by interacting with its C-terminal domain. This avoids photoactivation at low irradiance. In addition, it slows the OCP detachment from phycobilisomes by hindering fluorescence recovery protein interaction with bound OCP r . This maintains thermal dissipation of excess energy for a longer time. Pro-22, at the beginning of the N-terminal arm, has a key role in the correct positioning of the arm in OCP r , enabling strong OCP binding to phycobilisomes, but is not essential for photoactivation. Our results also show that the opening of the OCP during photoactivation is caused by the movement of the C-terminal domain with respect to the N-terminal domain and the N-terminal arm.Full sunlight is dangerous for plants, algae, and cyanobacteria. It can cause oxidative damages leading to the destruction of the photosynthetic apparatus and to cell death. A short-term photoprotective mechanism developed by oxygenic photosynthetic organisms is the reduction of excitation energy being funneled into the photochemical reaction centers by dissipating excess energy as heat at the level of the antennae (Niyogi and Truong, 2013). In plants and green algae, this mechanism involves the membrane chlorophyll antennae, the light-harvesting complex (for review, see Horton et al., 1996;Horton and Ruban, 2005;Jahns and Holzwarth, 2012), and in cyanobacteria, the extramembrane phycobiliprotein-containing antennae, the phycobilisomes (PBSs; for review, see Kirilovsky and Kerfeld, 2012;Kirilovsky, 2014). Despite these differences in composition and structure of their antennae, carotenoids have an essential role in both plants and cyanobacteria. In plants, high irradiance leads to acidification of the lumen that triggers conformational changes in the light-harvesting complexes and in their organization in the membrane, switching the light-harvesting complex into an effective energy-dissipating form. In cyanobacteria, high irradiance photoactivates a soluble carotenoid protein, the Orange Carotenoid Protein (OCP), that acts as the stress sensor and the energy quencher. In both cases, changes in pigment-pigment interactions (carotenoid-chlorophyll, carotenoid-bilin, chlorophyll-chlorophyll) enable thermal...