The photoactive Orange Carotenoid Protein (OCP) photoprotects cyanobacteria cells by quenching singlet oxygen and excess excitation energy. Its N-terminal domain is the active part of the protein, and the C-terminal domain regulates the activity. Recently, the characteristics of a family of soluble carotenoid-binding proteins (Helical Carotenoid Proteins [HCPs]), paralogs of the N-terminal domain of OCP, were described. Bioinformatics studies also revealed the existence of genes coding for homologs of CTD. Here, we show that the latter genes encode carotenoid proteins (CTDHs). This family of proteins contains two subgroups with distinct characteristics. One CTDH of each clade was further characterized, and they proved to be very good singlet oxygen quenchers. When synthesized in Escherichia coli or Synechocystis PCC 6803, CTDHs formed dimers that share a carotenoid molecule and are able to transfer their carotenoid to apo-HCPs and apo-OCP. The CTDHs from clade 2 have a cysteine in position 103. A disulfide bond is easily formed between the monomers of the dimer preventing carotenoid transfer. This suggests that the transfer of the carotenoid could be redox regulated in clade 2 CTDH. We also demonstrate here that apoOCPs and apo-CTDHs are able to take the carotenoid directly from membranes, while HCPs are unable to do so. HCPs need the presence of CTDH to become holo-proteins. We propose that, in cyanobacteria, the CTDHs are carotenoid donors to HCPs.Photosynthetic organisms performing oxygenic photosynthesis use solar energy, water, and inorganic carbon to produce all the organic molecules they need.Photosynthesis converts the absorbed energy into chemical energy and the reduction power necessary for the assimilation of CO 2 and the synthesis of organic carbon molecules. However, photosynthetic organisms cannot control the incoming flux of light, and too much light generates secondary reactions creating dangerous species of oxygen leading to cellular damage. Thus, in order to survive, photosynthetic organisms have developed a large variety of photoprotective mechanisms. One of them decreases the energy arriving at the reaction centers by increasing the thermal dissipation of excess excitation energy at the level of the antennae (for review, see Niyogi and Truong, 2013). In cyanobacteria, a soluble carotenoid protein, the Orange Carotenoid Protein (OCP), is essential for this mechanism, known as the OCP-related nonphotochemical quenching mechanism (Wilson et al., 2006; for review, see Kirilovsky and Kerfeld, 2016). In addition, OCP has a second photoprotective activity. It is a very good singlet oxygen ( 1 O 2 ) quencher (Kerfeld et al., 2003;Sedoud et al., 2014).OCP is a photoactive soluble carotenoid protein (Wilson et al., 2008). It is composed of two globular domains: an a-helical N-terminal domain (NTD; residues 18-165) that is unique to cyanobacteria and an a-helix/b-sheet C-terminal domain (CTD; residues