Abstract
The prokaryotic chemotaxis system is arguably the best-understood signaling pathway in biology. In all previously described species, chemoreceptors organize into a hexagonal (P6 symmetry) extended array. Here, we report an alternative symmetry (P2) of the chemotaxis apparatus that emerges from a strict linear organization of the histidine kinase CheA in Treponema denticola cells, which possesses arrays with the highest native curvature investigated thus far. Using cryo-ET, we reveal that Td chemoreceptor arrays assume an unusual arrangement of the supra-molecular protein assembly that has likely evolved to accommodate the high membrane curvature. The arrays have several 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. Furthermore, the previously characterized Td oxygen sensor ODP influences CheA ordering. These results suggest a greater diversity of the chemotaxis signaling system than previously thought.
Highlights
The prokaryotic chemotaxis system is arguably the best-understood signaling pathway in biology
We demonstrate the presence of an array architecture with two-fold (P2) symmetry in Treponema denticola (Td), which is likely caused by the high curvature of the cells
The spirochete chemotaxis system belongs to the F2 category, which has not been investigated with structural methods[14]
Summary
The prokaryotic chemotaxis system is arguably the best-understood signaling pathway in biology. The advent of so-called “mini-cell” bacterial strains produce extremely small cells that are ideal for cryo-ET8,10, and lipid-templating methods generate in vitro arrays with increased conformational homogeneity[11,12] These methods generate arrays with non-native curvature, and it is unclear how this may affect array structure and behavior. Cryo-ET analysis of Td cells lacking the oxygen sensor ODP reveals substantial changes in the ordering or mobility of CheA13. These data demonstrate a greater diversity of the chemotaxis system than previously realized and exemplify the importance of examining biological structures in native in vivo conditions
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