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Long-term positioning and polar preference of chemoreceptor clusters in E. coli.

ABSTRACT: The bacterial chemosensory arrays are a notable model for studying the basic principles of receptor clustering and cellular organization. Here, we provide a new perspective regarding the long-term dynamics of these clusters in growing E. coli cells. We demonstrate that pre-existing lateral clusters tend to avoid translocation to pole regions and, therefore, continually shuttle between the cell poles for many generations while being static relative to the local cell-wall matrix. We also show that the polar preference of clusters results fundamentally from reduced clustering efficiency in the lateral region, rather than a developmental-like progression of clusters. Furthermore, polar preference is surprisingly robust to structural alterations designed to probe preference due to curvature sorting, perturbing the cell envelope physiology affects the cluster-size distribution, and the size-dependent mobility of receptor complexes differs between polar and lateral regions. Thus, distinct envelope physiology in the polar and lateral cell regions may contribute to polar preference.

SUBMITTER: Koler M

PROVIDER: S-EPMC6202326 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Long-term positioning and polar preference of chemoreceptor clusters in E. coli.

Koler Moriah M Peretz Eliran E Aditya Chetan C Shimizu Thomas S TS Vaknin Ady A

Nature communications 20181025 1

The bacterial chemosensory arrays are a notable model for studying the basic principles of receptor clustering and cellular organization. Here, we provide a new perspective regarding the long-term dynamics of these clusters in growing E. coli cells. We demonstrate that pre-existing lateral clusters tend to avoid translocation to pole regions and, therefore, continually shuttle between the cell poles for many generations while being static relative to the local cell-wall matrix. We also show that ...[more]

PMID: 30361683

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Project description:Chemoreceptors are localized at the cell poles of Escherichia coli and other rod-shaped bacteria. Over the years, different mechanisms have been put forward to explain this polar localization, including stochastic clustering, membrane curvature-driven localization, interactions with the Tol-Pal complex, and nucleoid exclusion. To evaluate these mechanisms, we monitored the cellular localization of the aspartate chemoreceptor Tar in different deletion mutants. We did not find any indication for either stochastic cluster formation or nucleoid exclusion. However, the presence of a functional Tol-Pal complex appeared to be essential to retain Tar at the cell poles. Interestingly, Tar still accumulated at midcell in tol and in pal deletion mutants. In these mutants, the protein appears to gather at the base of division septa, a region characterized by strong membrane curvature. Chemoreceptors, like Tar, form trimers of dimers that bend the cell membrane due to a rigid tripod structure. The curvature approaches the curvature of the cell membrane generated during cell division, and localization of chemoreceptor tripods at curved membrane areas is therefore energetically favorable, as it lowers membrane tension. Indeed, when we introduced mutations in Tar that abolish the rigid tripod structure, the protein was no longer able to accumulate at midcell or the cell poles. These findings favor a model where chemoreceptor localization in E. coli is driven by strong membrane curvature and association with the Tol-Pal complex.IMPORTANCE Bacteria have exquisite mechanisms to sense and adapt to the environment they live in. One such mechanism involves the chemotaxis signal transduction pathway, in which chemoreceptors specifically bind certain attracting or repelling molecules and transduce the signals to the cell. In different rod-shaped bacteria, these chemoreceptors localize specifically to cell poles. Here, we examined the polar localization of the aspartate chemoreceptor Tar in E. coli and found that membrane curvature at cell division sites and the Tol-Pal protein complex localize Tar at cell division sites, the future cell poles. This study shows how membrane curvature can guide localization of proteins in a cell.

Dataset Information

Long-term positioning and polar preference of chemoreceptor clusters in E. coli.

Publications

Long-term positioning and polar preference of chemoreceptor clusters in E. coli.

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