Chromatic adaptation (CA) in cyanobacteria has provided a model system for the study of the environmental control of photophysiology for several decades. All forms of CA that have been examined so far (types II and III) involve changes in the relative contents of phycoerythrin (PE) and/or phycocyanin when cells are shifted from red to green light and vice versa. However, the chromophore compositions of these polypeptides are not altered. Some marine Synechococcus species strains, which possess two PE forms (PEI and PEII), carry out another type of CA (type IV), occurring during shifts from blue to green or white light. Two chromatically adapting strains of marine Synechococcus recently isolated from the Gulf of Mexico were utilized to elucidate the mechanism of type IV CA. During this process, no change in the relative contents of PEI and PEII was observed. Instead, the ratio of the two chromophores bound to PEII, phycourobilin and phycoerythrobilin, is high under blue light and low under white light. Mass spectroscopy analyses of isolated PEII ␣-and ␤-subunits show that there is a single PEII protein type under all light climates. The CA process seems to specifically affect the chromophorylation of the PEII (and possibly PEI) ␣ chain. We propose a likely process for type IV CA, which involves the enzymatic activity of one or several phycobilin lyases and/or lyase-isomerases differentially controlled by the ambient light quality. Phylogenetic analyses based on the 16S rRNA gene confirm that type IV CA is not limited to a single clade of marine Synechococcus.Members of the genus Synechococcus are ubiquitous and ecologically important in marine ecosystems (19,24,28). This form genus, which includes freshwater, obligatory marine, and halotolerant strains, is clearly polyphyletic. However, based on 16S rRNA gene sequence analysis, most obligatory marine representatives fall into a single monophyletic group called "subcluster 5.1," previously termed "marine cluster A" (8,14). Like most other cyanobacteria, all members of Synechococcus subcluster 5.1 (hereinafter referred to as "marine Synechococcus") utilize phycobilisomes (PBSs) as their major light-harvesting antenna system. PBSs are large macromolecular complexes that consist of a core in direct contact with the stromal surface of the thylakoid membrane, and this core is surrounded by six radiating rods. The major constituents of PBSs are several classes of chromophore-binding proteins called phycobiliproteins (PBPs). In all PBS-containing cyanobacteria, the PBP components of the core and proximal parts of the rods are allophycocyanin (AP) and phycocyanin (PC), respectively. The PBP components constituting the distal parts of rods are more varied. All marine Synechococcus sp. strains but those belonging to clades VI and VIII (8) are thought to possess two different phycoerythrin (PE) forms, termed PEI and PEII. The latter is specific to this cyanobacterial group and is located at a distal position within the rods. Each PBP binds one or two types of chromophores (p...