[Introduction] Page 2 of 20 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 cell ular functions in plants, bacteria, and fungi. 1-9 Bacterial phytochro mes consist of a photosensory core and a C-te rminal regulatory domain. 10,11 Structures of photosensory cores are reported in the resting state 12-18 and conformational responses to light activat ion have been proposed in the vicinity of the chromophore. 19-23 However, the structure of the signalling state and the mechanism of downstream signal re lay through the photosensory core remain elusive. Here, we report crystal and solution structures of the resting and active states of the photosensory core of the bacteriophytochrome from Deinococcus radiodurans . The structures reveal an open and closed form of the dimeric protein for the signalling an d resting state, 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 unus ual mechanism where atomic scale conformational ch anges around the chromopho re are first amplified into an Ångström scale distance change in the tongue, and further grow into a nanometre scale conformational sign al. The structural mechanism is a blueprint for understanding how the sensor proteins connect to the cellular signalling network.