Baseplate variability of Vibrio cholerae chemoreceptor arrays

Abstract

The chemoreceptor array, a remarkably ordered supramolecular complex, is composed of hexagonally packed trimers of receptor dimers networked by a histidine kinase and one or more coupling proteins. Even though the receptor packing is universal among chemotactic bacteria and archaea, the array architecture has been extensively studied only in selected model organisms. Here, we show that even in the complete absence of the kinase, the cluster II arrays in Vibrio cholerae retain their native spatial localization and the iconic hexagonal packing of the receptors with 12-nm spacing. Our results demonstrate that the chemotaxis array is versatile in composition, a property that allows auxiliary chemotaxis proteins such as ParP and CheV to integrate directly into the assembly. Along with its compositional variability, cluster II arrays exhibit a low degree of structural stability compared with the ultrastable arrays in Escherichia coli. We propose that the variability in chemoreceptor arrays is an important mechanism that enables the incorporation of chemotaxis proteins based on their availability.

Atypical chemoreceptor arrays accommodate high membrane curvature

“…Previous studies in Ec and Vc demonstrate that the chemotaxis arrays can accommodate vastly different curvatures between lysed and artificially small mini-cell strains 8,19,20 . However, Td cells demonstrate a significantly higher curvature of the cell membrane than organisms investigated for their chemotaxis arrangement thus far 4,8,19 . As a measure of comparison, the Vc mini-cells used in a previous study have an inner membrane curvature of 9.15 +/- 4.5 /µm (radius 1092 Å, n = 6 cells), and the Td cells have an inner membrane curvature of 35.8 +/- 6.6 /µm (radius: 279 Å, n = 10 cells) (Fig.…”

“…In this system, three proteins comprise the rings at the receptor tips: CheA, CheW, and a CheW-CheR like protein. Like the Ec system, these proteins in Td are integrated into the array with strict organization 8,19 . However, a new linear arrangement of CheA is present that generates ‘strands’ of rings interlinked by the CheA dimerization domain (P3).…”

“…Therefore, it is likely that the behavior and characteristics of chemoreceptor arrays in general can be influenced by perturbing the shape of the cell membrane. Importantly, previous cryo-ET chemotaxis studies have relied on artificial systems for higher resolution data, but these methods generate arrays with non-native curvature 8,17,20,21 . Collectively, these data exemplify the importance of examining biological structures in native in vivo conditions, as essential cellular features may not be recapitulated under in vitro, ex vivo , and artificial systems.…”

“…For example, many bacteria contain multiple copies of CheW, with some fused to other protein modules (i.e. CheV), and in vivo analyses of Vibrio cholerae ( Vc ) chemotaxis arrays have revealed that CheA and CheW in the rings apparently lack an ordered arrangement 8,9 .…”

Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system

“…A novel chemosensory array in V. cholerae and P. aeruginosa in limited growth conditions Previously, we used cryo-ET to reveal the structure of two types of chemosensory arrays in V. cholerae. When grown in rich medium, the cells contain a polarly-localized membrane-bound array, with a distance of 25 nm between the inner membrane (IM) and the baseplate, composed of kinase and scaffold proteins (11,15). We analysis predicts three chemosensory gene clusters, one each from the F6 (MEALZ_3148 -MEALZ_3158), F7 (MEALZ_2869-MEALZ_2879) and F8 classes (MEALZ_2939 -MEALZ_2942, Table S2).…”