The cyanobacterium Synechococcus elongatus is a model organism for the study of circadian rhythms. It is naturally competent for transformation-that is, it takes up DNA from the environment, but the underlying mechanisms are unclear. Here, we use a genome-wide screen to identify genes required for natural transformation in S. elongatus, including genes encoding a conserved Type IV pilus, genes known to be associated with competence in other bacteria, and others. Pilus biogenesis occurs daily in the morning, while natural transformation is maximal when the onset of darkness coincides with the dusk circadian peak. Thus, the competence state in cyanobacteria is regulated by the circadian clock and can adapt to seasonal changes of day length.

Natural genetic competence-based transformation contributed to the evolution of prokaryotes, including the cyanobacterial phylum that established oxygenic photosynthesis. The cyanobacterium Synechococcus elongatus is noted both as a model system for analyzing a prokaryotic circadian clock and for its facile, but poorly understood, natural competence. Here a genome-wide screen aimed at determining the genetic basis of competence in cyanobacteria identified all genes required for natural transformation in S. elongatus, including conserved Type IV pilus, competence-associated, and newly described genes, and revealed that the circadian clock controls the process. The findings uncover a daily program that determines the state of competence in S. elongatus and adapts to seasonal changes of day-length. Pilus biogenesis occurs daily in the morning, but competence is maximal upon the coincidence of circadian dusk and the onset of darkness. As in heterotrophic bacteria, where natural competence is conditionally regulated by nutritional or other stress, cyanobacterial competence is conditional and is tied to the daily cycle set by the cell’s most critical nutritional source, the Sun.