Atypical chemoreceptor arrays accommodate high membrane curvature

Abstract/SummaryThe prokaryotic chemotaxis system is arguably the best-understood signaling pathway in biology, but most insights have been obtained from only a few model organisms and many studies have relied on artificial systems that alter membrane curvature1-3. In all previously described species, chemoreceptors organize with the histidine kinase (CheA) and coupling protein (CheW) into a hexagonal (P6 symmetry) extended array that is considered universal among archaea and bacteria4,5. Here, for the first time, we report an alternative symmetry (P2) of the chemotaxis apparatus that emerges from a strict linear organization of CheA in Treponema denticola cells, which possesses arrays with the highest native curvature investigated thus far. Using cryo-ET, we reveal that the Td chemoreceptor arrays assume a truly unusual arrangement of the supra-molecular protein assembly that has likely evolved to accommodate the high membrane curvature. The arrays have several additional atypical features, such as an extended dimerization domain of CheA and a variant CheW-CheR-like fusion protein that is critical for maintaining an ordered chemosensory apparatus in an extremely curved cell. Furthermore, the previously characterized Td oxygen sensor ODP influences array integrity and its loss substantially orders CheA. These results suggest a greater diversity of the chemotaxis signaling system than previously thought and demonstrate the importance of examining transmembrane systems in vivo to retain native membrane curvature.