Phytochromes sense red/far-red light and control many biological processes in plants, fungi, and bacteria. Although crystal structures of dark and light adapted states have been determined, the molecular mechanisms underlying photoactivation remains elusive. Here we demonstrate that the conserved tongue region of the PHY domain of a 57kDa photosensory module of Deinococcus radiodurans phytochrome, changes from a structurally heterogeneous dark state to an ordered light activated state. The results were obtained in solution by utilizing a laser-triggered activation approach detected on the atomic level with high-resolution protein NMR spectroscopy. The data suggest that photosignaling of phytochromes relies on careful modulation of structural heterogeneity of the PHY tongue.