Sensory rhodopsin II, the photophobic receptor from Natronomonas pharaonis (NpSRII)5, forms a 2:2 complex with its cognate transducer (N. pharaonis halobacterial transducer of rhodopsins II (NpHtrII)) in lipid membranes. Light activation of NpSRII leads to a displacement of helix F, which in turn triggers a rotation/screw-like motion of TM2 in NpHtrII. This conformational change is thought to be transmitted through the membrane adjacent conserved signal transduction domain in histidine kinases, adenylyl cyclases, methyl-accepting chemotaxis proteins, and phosphatases (HAMP domain) to the cytoplasmic signaling domain of the transducer. The architecture and function of the HAMP domain are still unknown. In order to obtain information on the structure and dynamics of this region, EPR experiments on a truncated transducer (NpHtrII(157)) and NpSRII, site-directed spin-labeled and reconstituted into purple membrane lipids, have been carried out. A nitroxide scanning involving residues in the transducer helix TM2, in the predicted AS-1 region, and at selected positions in the following connector and AS-2 regions of the HAMP domain has been performed. Accessibility and dynamics data allowed us to identify a helical region up to residue Ala(94) in the AS-1 amphipathic sequence, followed by a highly dynamic domain protruding into the water phase. Additionally, transducer-transducer and transducer-receptor proximity relations revealed the overall architecture of the AS-1 sequences in the 2:2 complex, which are suggested to form a molten globular type of a coiled-coil bundle.