Positioning of chemosensory clusters in E. coli and its relation to cell division

Thiem, Sebastian; Kentner, David; Sourjik, Victor

doi:10.1038/sj.emboj.7601610

Cited by 97 publications

(131 citation statements)

References 61 publications

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“…All three methods detect no more than a few patches per cell, with most (~80%) located at a cell pole, although not at any particular position along the polar membrane. Non-polar, lateral patches are distributed at future division sites [21]. There is no evidence for functional differences between polar and lateral patches.…”

Section: Patches Provide the Physical Organization In Which Functionamentioning

confidence: 92%

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Bacterial chemoreceptors: high-performance signaling in networked arrays

Hazelbauer

Falke

Parkinson

2008

Trends in Biochemical Sciences

573

804

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Chemoreceptors are crucial components in the bacterial sensory systems that mediate chemotaxis. Chemotactic responses exhibit exquisite sensitivity, extensive dynamic range and precise adaptation. The mechanisms that mediate these high-performance functions involve not only actions of individual proteins but also interactions among clusters of components, localized in extensive patches of thousands of molecules. Recently, these patches have been imaged in native cells, important features of chemoreceptor structure and on-off switching have been identified, and new insights have been gained into the structural basis and functional consequences of higher order interactions among sensory components. These new data suggest multiple levels of molecular interactions, each of which contribute specific functional features and together create a sophisticated signaling device. High-performance signaling in bacterial chemotaxisThe high-performance chemotaxis signaling system of Escherichia coli (Box 1) involves a limited number of components but notable sophistication [1][2][3][4]. This system has become a paradigm for molecular characterization of biological signaling mechanisms. Transmembrane chemoreceptors, known as methyl-accepting chemotaxis proteins (MCPs), direct cell locomotion by regulating the histidine kinase CheA; CheA phosphorylates a response regulator, which in turn controls the rotational direction of the flagellar motor. Chemotactic sensitivity and the range of signal detection are regulated by adaptational modification of chemoreceptors via reversible glutamyl methylation. The resulting interplay between motor control and sensory adaptation produces directed motile behavior. E. coli chemoreceptors are the most extensively studied representatives of the MCP super-family, central components of homologous systems that mediate tactic responses [5,6] across the phylogenetic diversity of bacteria and archaea [7].In E. coli chemotaxis proteins cluster in membrane-associated patches [8]. Interaction within patches is thought to contribute to notable features of the signaling system: high sensitivity, wide dynamic range, extensive cooperativity and precise adaptation. Delineating the molecular mechanisms underlying these features will require knowledge of structures of the components, complexes and higher order arrays. In addition it will require definition of organization at the multiple levels of interaction among signaling components and an understanding of the changes in components and their interactions that mediate signaling at each level. In the past few years, notable progress has been made toward acquiring the NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript information and insights necessary for understanding these molecular mechanisms. This review describes that progress. Here we follow the lead of most investigators in the area, and do not distinguish between studies of first cousins E. coli and Salmonella enterica serovar Typhimurium. Thus, referenc...

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Section: Patches Provide the Physical Organization In Which Functionamentioning

confidence: 92%

“…There is no evidence for functional differences between polar and lateral patches. Patches in the polar area are mobile within the curvature of the pole but lateral patches appear fixed [21]. Polar localization is a separate phenomenon from formation of focused patches.…”

Section: Patches Provide the Physical Organization In Which Functionamentioning

confidence: 95%

Bacterial chemoreceptors: high-performance signaling in networked arrays

Hazelbauer

Falke

Parkinson

2008

Trends in Biochemical Sciences

573

804

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“…MCPs likely are inserted at random sites throughout the cell membrane and then are subject to diffusion-mediated clustering that results in the recruitment of additional chemotaxis proteins (6,9,(33)(34)(35)(36). Because V. parahaemolyticus chemotaxis proteins form randomly localized clusters in the absence of ParC and ParP, it is likely that such a diffusion-mediated mechanism also contributes to the assembly of the V. parahaemolyticus chemotactic machinery.…”

Section: Discussionmentioning

confidence: 99%

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

Ringgaard

Zepeda-Rivera

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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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.

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“…Chemoreceptor clusters are predominantly polar (Maddock and Shapiro, 1993), but a few are regularly positioned along the cell body (Sourjik and Armitage, 2010). This periodic arrangement is spontaneous: chemoreceptors stochastically self-assemble in a concentration-dependent manner to build new clusters or to expand old ones, and the formation of new clusters is entropically favored far away from pre-existing ones (Thiem et al, 2007;Thiem and Sourjik, 2008;Wang et al, 2008;Greenfield et al, 2009). As a consequence of this organization, larger clusters appear confined to future division sites (Thiem et al, 2007).…”

Section: Growth-dependent Transmission From the Sidewallmentioning

confidence: 99%

“…This periodic arrangement is spontaneous: chemoreceptors stochastically self-assemble in a concentration-dependent manner to build new clusters or to expand old ones, and the formation of new clusters is entropically favored far away from pre-existing ones (Thiem et al, 2007;Thiem and Sourjik, 2008;Wang et al, 2008;Greenfield et al, 2009). As a consequence of this organization, larger clusters appear confined to future division sites (Thiem et al, 2007). This progressively leads to their polar accumulation and retention after several generations.…”

Section: Growth-dependent Transmission From the Sidewallmentioning

confidence: 99%

How do bacteria localize proteins to the cell pole?

Laloux

Jacobs‐Wagner

2014

Journal of Cell Science

157

158

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It is now well appreciated that bacterial cells are highly organized, which is far from the initial concept that they are merely bags of randomly distributed macromolecules and chemicals. Central to their spatial organization is the precise positioning of certain proteins in subcellular domains of the cell. In particular, the cell poles -the ends of rod-shaped cells -constitute important platforms for cellular regulation that underlie processes as essential as cell cycle progression, cellular differentiation, virulence, chemotaxis and growth of appendages. Thus, understanding how the polar localization of specific proteins is achieved and regulated is a crucial question in bacterial cell biology. Often, polarly localized proteins are recruited to the poles through their interaction with other proteins or protein complexes that were already located there, in a so-called diffusion-and-capture mechanism. Bacteria are also starting to reveal their secrets on how the initial pole 'recognition' can occur and how this event can be regulated to generate dynamic, reproducible patterns in time (for example, during the cell cycle) and space (for example, at a specific cell pole). Here, we review the major mechanisms that have been described in the literature, with an emphasis on the self-organizing principles. We also present regulation strategies adopted by bacterial cells to obtain complex spatiotemporal patterns of protein localization.

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Positioning of chemosensory clusters in E. coli and its relation to cell division

Cited by 97 publications

References 61 publications

Bacterial chemoreceptors: high-performance signaling in networked arrays

Bacterial chemoreceptors: high-performance signaling in networked arrays

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

How do bacteria localize proteins to the cell pole?

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