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

Moriah Koler,Eliran Peretz,Chetan Aditya,Ady Vaknin,Thomas S Shimizu

doi:10.1038/s41467-018-06835-5

Moriah Koler, Eliran Peretz + Show 3 more

Open Access

https://doi.org/10.1038/s41467-018-06835-5

Copy DOI

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.

Highlights

The bacterial chemosensory arrays are a notable model for studying the basic principles of receptor clustering and cellular organization
We found that the prominent effect of the the peptidoglycan matrix (TolA) deletion on chemoreceptor clustering is an overall fragmentation of receptor clusters; in the absence of TolA, the clusters were typically smaller but approximately threefold more clusters per cell were observed (Fig. 6a)
By following the long-term positional dynamics of chemoreceptor clusters, we identified two distinct behaviors (Fig. 7a): clusters that nucleated directly at the cell pole during or after cell division remained polar in future generations, and clusters that nucleated at the lateral region mostly remained lateral and as the cell underwent cycles of elongation and division continued to shuttle between the cell poles

Summary

Introduction

The bacterial chemosensory arrays are a notable model for studying the basic principles of receptor clustering and cellular organization. E. coli chemoreceptors were among the first membrane-bound bacterial proteins that were shown to form large clusters with a clear polar preference[3,4], and such chemosensory clusters were later found in many other motile bacteria[5]. We demonstrate that lateral clusters tend to avoid translocation to the new cell pole regions after cell division and keep shuttling between the cell poles Quantitative analysis of their positional dynamics indicates that lateral clusters tend to be static relative to the local cell-wall matrix for many generations, at least, along the long axis of the cell. Chloramphenicol, which leads to nucleoid condensation, and TolA, which connects the cytoplasmic membrane with the cell-wall matrix, can affect receptor clustering By their nature, such effectors can lead to distinct local environments in the polar and lateral regions. We find that the manner in which the mobility of receptor complexes depends on their size differs between the polar and lateral regions, which can potentially contribute to the observed polar bias

Methods

Results

Conclusion