Universal architecture of bacterial chemoreceptor arrays

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333

The chemoreceptors of Escherichia coli localize to the cell poles and form a highly ordered array in concert with the CheA kinase and the CheW coupling factor. However, a high-resolution structure of the array has been lacking, and the molecular basis of array assembly has thus remained elusive. Here, we use cryoelectron tomography of flagellated E. coli minicells to derive a 3D map of the intact array. Docking of high-resolution structures into the 3D map provides a model of the core signaling complex, in which a CheA/CheW dimer bridges two adjacent receptor trimers via multiple hydrophobic interactions. A further, hitherto unknown, hydrophobic interaction between CheW and the homologous P5 domain of CheA in an adjacent core complex connects the complexes into an extended array. This architecture provides a structural basis for array formation and could explain the high sensitivity and cooperativity of chemotaxis signaling in E. coli.

mentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells

Li¹,

Morado

et al. 2012

181

333

“…In Escherichia coli and many other bacteria, signaling complexes involve stable noncovalent interactions among transmembrane bacterial chemoreceptors, histidine kinase CheA and coupling protein CheW. In vivo, signaling complexes appear as arrays that can contain tens to thousands of these components (3,4). In the extensively characterized systems of E. coli and Salmonella enterica, arrays include several different kinds of chemoreceptors, each able to recognize one or a few specific attractants and repellents.…”

mentioning

confidence: 99%

Selective allosteric coupling in core chemotaxis signaling complexes

Hazelbauer

2014

Bacterial chemotaxis is mediated by signaling complexes that sense chemical gradients and direct bacteria to favorable environments by controlling a histidine kinase as a function of chemoreceptor ligand occupancy. Core signaling complexes contain two trimers of transmembrane chemoreceptor dimers, each trimer binding a coupling protein CheW and a protomer of the kinase dimer. Core complexes assemble into hexagons, and these form hexagonal arrays. The notable cooperativity and amplification in bacterial chemotaxis is thought to reflect allosteric interactions in cores, hexagons, and arrays, but little is known about this presumed allostery. We investigated allostery in core complexes assembled with two chemoreceptor species, each recognizing a different ligand. Chemoreceptors were inserted in Nanodiscs, which rendered them water soluble and allowed isolation of individual complexes. Neighboring dimers in receptor trimers influenced one another's operational ligand affinity, indicating allosteric coupling. However, this coupling did not include the key function of kinase inhibition. Our data indicated that only one receptor dimer could inhibit kinase as a function of ligand occupancy. This selective allosteric coupling corresponded with previously identified structural asymmetry: only one dimer in a trimer contacts kinase and only one CheW. We suggest one of these dimers couples ligand occupancy to kinase inhibition. Additionally, we found that kinase protomers are allosterically coupled, conveying inhibition across the dimer interface. Because kinase dimers connect core complex hexagons, allosteric communication across dimer interfaces provides a pathway for receptor-generated kinase inhibition in one hexagon to spread to another, providing a crucial step for the extensive amplification characteristic of chemotactic signaling.transmembrane receptors | bacterial chemotaxis | allosteric coupling | histidine kinases | Nanodiscs

“…Chemosensory proteins are found universally in large macromolecular clusters known as "chemotactic signaling arrays" (2)(3)(4)(5). MCPs, together with CheA and CheW, form the sensory core of these clusters.…”

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confidence: 99%

ParP prevents dissociation of CheA from chemotactic signaling arrays and tethers them to a polar anchor

Ringgaard

Zepeda-Rivera

et al. 2013

Significance Targeting of cellular components to a particular site in a cell is often a highly regulated process, even in cells as small as bacteria. Robust chemotactic signaling, which is used by motile bacteria to survey their environments and navigate in response to them, requires appropriate cellular distribution of a large chemosensory apparatus. Here, we report how polarly flagellated vibrios ensure polar localization of their chemotactic machinery by capturing signaling proteins at the pole. Polar localization is mediated by a tripartite protein interaction network in which one protein prevents disassociation of a key signaling component from chemotactic complexes and tethers the complexes to a polar anchor. Polar tethering and localization are prerequisites for proper chemotaxis.