The solution and crystal structures of a bacterial phytochrome photosensory core in both its resting and activated states are determined; switching between closed (resting) and open (activated) forms is found to be mediated by a conserved ‘tongue’, and the structures indicate that smaller changes in the vicinity of the chromophore are amplified in scale as they are transmitted through the tongue and beyond. The crystal structure of the photosensory core of a bacterial phytochrome in both the resting and the active (illuminated) state has now been solved. Working with the phytochrome from the extremophile Deinococcus radiodurans, Sebastian Westenhoff and colleagues demonstrate that toggling between resting and active forms is mediated by a conserved 'tongue' that contacts the chromophore. Atomic-scale structural changes in the vicinity of the chromophore are amplified as they are transmitted through the tongue and beyond, culminating in a nanometre-scale conformational signal that feeds into the rest of the cellular signalling network. Sensory proteins must relay structural signals from the sensory site over large distances to regulatory output domains. Phytochromes are a major family of red-light-sensing kinases that control diverse cellular functions in plants, bacteria and fungi1,2,3,4,5,6,7,8,9. Bacterial phytochromes consist of a photosensory core and a carboxy-terminal regulatory domain10,11. Structures of photosensory cores are reported in the resting state12,13,14,15,16,17,18 and conformational responses to light activation have been proposed in the vicinity of the chromophore19,20,21,22,23. However, the structure of the signalling state and the mechanism of downstream signal relay through the photosensory core remain elusive. Here we report crystal and solution structures of the resting and activated states of the photosensory core of the bacteriophytochrome from Deinococcus radiodurans. The structures show an open and closed form of the dimeric protein for the activated and resting states, respectively. This nanometre-scale rearrangement is controlled by refolding of an evolutionarily conserved ‘tongue’, which is in contact with the chromophore. The findings reveal an unusual mechanism in which atomic-scale conformational changes around the chromophore are first amplified into an ångstrom-scale distance change in the tongue, and further grow into a nanometre-scale conformational signal. The structural mechanism is a blueprint for understanding how phytochromes connect to the cellular signalling network.