Ramlibacter tataouinensis TTB310, a non-photosynthetic betaproteobacterium isolated from a semi-arid region of southern Tunisia, forms both rods and cysts. Cysts are resistant to desiccation and divide when water and nutrients are available. Rods are motile and capable of dissemination. Due to the strong correlation between sunlight and desiccation, light is probably an important external signal for anticipating desiccating conditions. Six genes encoding potential light sensors were identified in strain TTB310. Two genes encode for bacteriophytochromes, while the four remaining genes encode for putative blue light receptors. We determined the spectral and photochemical properties of the two recombinant bacteriophytochromes RtBphP1 and RtBphP2. In both cases, they act as sensitive red light detectors. Cyst divisions and a complete cyst-rod-cyst cycle are the main processes in darkness, whereas rod divisions predominate in red or far-red light. Mutant phenotypes caused by the inactivation of genes encoding bacteriophytochromes or heme oxygenase clearly show that both bacteriophytochromes are involved in regulating the rod-rod division. This process could favor rapid rod divisions at sunrise, after dew formation but before the progressive onset of desiccation. Our study provides the first evidence of a light-based strategy evolved in a non-photosynthetic bacterium to exploit scarse water in a desert environment.