We have examined the molecular and photosynthetic responses of a planktonic cyanobacterium to shifts in light intensity over periods up to one generation (7 h). Synechococcus sp. PCC 7942 possesses two functionally distinct forms of the D1 protein, D1:1 and D1:2. Photosystem II (PSII) centers containing D1:1 are less efficient and more susceptible to photoinhibition than are centers containing D1:2, Under 50 mu mol photons m(-2). s(-1), PSII centers contain D1:1, but upon shifts to higher light (200 to 1000 mu mol photons m(-2). s(-1)), D1:1 is rapidly replaced by D1:2, with the rate of interchange dependent on the magnitude of the light shift. This interchange is readily reversed when cells are returned to 50 mu mol photons m(-2). s(-1). If, however, incubation under 200 mu mol photons m(-2). s(-1) is extended, D1:1 content recovers and by 3 h after the light shift D1:1 once again predominates. Oxygen evolution and chlorophyll (Chi) fluorescence measurements spanning the light shift and D1 interchanges showed an initial inhibition of photosynthesis at 200 mu mol photons m(-2). s(-1), which correlates with a proportional loss of total D1 protein and a cessation of growth. This was followed by recovery in photosynthesis and growth as the maximum level of D1:2 is reached after 2 h at 200 mu mol photons m(-2). s(-1) Thereafter, photosynthesis steadily declines with the loss of D1:2 and the return of the less-efficient D1:1. During the D1:1/D1:2 interchanges, no significant change occurs in the level of phycocyanin (PC) and Chl a, nor of the phycobilisome rod linkers. Nevertheless, the initial PC/Chl a ratio strongly influences the magnitude of photoinhibition and recovery during the light shifts. In Synechococcus sp. PCC 7942, the PC/Chl a ratio responds only slowly to light intensity or quality, while the rapid but transient interchange between D1:1 and D1:2 modulates PSII activity to limit damage upon exposure to excess light.