In halophilic archaea the photophobic response
is mediated by the membrane-embedded 2:2 photoreceptor/-
transducer complex SRII/HtrII, the latter being homologous
to the bacterial chemoreceptors. Both systems bias the rotation
direction of the flagellar motor via a two-component system
coupled to an extended cytoplasmic signaling domain formed
by a four helical antiparallel coiled-coil structure. For signal
propagation by the HAMP domains connecting the transmembrane and cytoplasmic domains, it was suggested that a
two-state thermodynamic equilibrium found for the first
HAMP domain in NpSRII/NpHtrII is shifted upon activation, yet signal propagation along the coiled-coil transducer remains
largely elusive, including the activation mechanism of the coupled kinase CheA. We investigated the dynamic and structural
properties of the cytoplasmic tip domain of NpHtrII in terms of signal transduction and putative oligomerization using sitedirected spin labeling electron paramagnetic resonance spectroscopy. We show that the cytoplasmic tip domain of NpHtrII is
engaged in a two-state equilibrium between a dynamic and a compact conformation like what was found for the first HAMP
domain, thus strengthening the assumption that dynamics are the language of signal transfer. Interspin distance measurements in
membranes and on isolated 2:2 photoreceptor/transducer complexes in nanolipoprotein particles provide evidence that archaeal
photoreceptor/-transducer complexes analogous to chemoreceptors form trimers-of-dimers or higher-order assemblies even in
the absence of the cytoplasmic components CheA and CheW, underlining conservation of the overall mechanistic principles
underlying archaeal phototaxis and bacterial chemotaxis systems. Furthermore, our results revealed a significant influence of the
NpHtrII signaling domain on the NpSRII photocycle kinetics, providing evidence for a conformational coupling of SRII and
HtrII in these complexes.