All microbes must contend with fluctuations in growth conditions, but photosynthetic bacteria face a special challenge of predictable cycles of energy availability set by the rotation of the Earth. Cyanobacteria have developed mechanisms to respond to and anticipate the day-night cycle using an internal 24-hour oscillator based on protein phosphorylation. Many features of this system can be reconstituted using purified proteins, including the ability to respond to seasonal changes in day length. We show that cyanobacterial physiology undergoes dramatic daily remodeling that is regulated by the clock, including reversible separation of a special subset of the proteome into condensed puncta during the night.