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Title: Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy

Abstract

The Escherichia coli chemotaxis network is a model system for biological signal processing. In E. coli, transmembrane receptors responsible for signal transduction assemble into large clusters containing several thousand proteins. These sensory clusters have been observed at cell poles and future division sites. Despite extensive study, it remains unclear how chemotaxis clusters form, what controls cluster size and density, and how the cellular location of clusters is robustly maintained in growing and dividing cells. Here, we use photoactivated localization microscopy (PALM) to map the cellular locations of three proteins central to bacterial chemotaxis (the Tar receptor, CheY, and CheW) with a precision of 15 nm. We find that cluster sizes are approximately exponentially distributed, with no characteristic cluster size. One-third of Tar receptors are part of smaller lateral clusters and not of the large polar clusters. Analysis of the relative cellular locations of 1.1 million individual proteins (from 326 cells) suggests that clusters form via stochastic self-assembly. The super-resolution PALM maps of E. coli receptors support the notion that stochastic self-assembly can create and maintain approximately periodic structures in biological membranes, without direct cytoskeletal involvement or active transport.

Authors:
 [1];  [2];  [3];  [4];  [5];  [3];  [1]
+ Show Author Affiliations
  1. University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  2. University of California, Berkeley, CA (United States)
  3. Howard Hughes Medical Institute, Janelia Farm Research Campus, Ashburn, VA (United States)
  4. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
  5. Princeton University, NJ (United States
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Fusion Energy Sciences (FES); Sloan and Searle Foundations; National Institutes of Health (NIH)
OSTI Identifier:
1627160
Grant/Contract Number:  
AC02-05CH11231; R01 GM77856; R01 GM084716; R01 GMO73186
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Biology (Online)
Additional Journal Information:
Journal Name: PLoS Biology (Online); Journal Volume: 7; Journal Issue: 6; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; chemotaxis; tar; membrane receptor signaling; cell polarity; cell fusion; molecular self assembly; nucleation; bacteria

Citation Formats

Greenfield, Derek, McEvoy, Ann L., Shroff, Hari, Crooks, Gavin E., Wingreen, Ned S., Betzig, Eric, and Liphardt, Jan. Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy. United States: N. p., 2009. Web. doi:10.1371/journal.pbio.1000137.
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Greenfield, Derek, McEvoy, Ann L., Shroff, Hari, Crooks, Gavin E., Wingreen, Ned S., Betzig, Eric, & Liphardt, Jan. Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy. United States. https://doi.org/10.1371/journal.pbio.1000137
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Greenfield, Derek, McEvoy, Ann L., Shroff, Hari, Crooks, Gavin E., Wingreen, Ned S., Betzig, Eric, and Liphardt, Jan. Tue . "Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy". United States. https://doi.org/10.1371/journal.pbio.1000137. https://www.osti.gov/servlets/purl/1627160.
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@article{osti_1627160,
title = {Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy},
author = {Greenfield, Derek and McEvoy, Ann L. and Shroff, Hari and Crooks, Gavin E. and Wingreen, Ned S. and Betzig, Eric and Liphardt, Jan},
abstractNote = {The Escherichia coli chemotaxis network is a model system for biological signal processing. In E. coli, transmembrane receptors responsible for signal transduction assemble into large clusters containing several thousand proteins. These sensory clusters have been observed at cell poles and future division sites. Despite extensive study, it remains unclear how chemotaxis clusters form, what controls cluster size and density, and how the cellular location of clusters is robustly maintained in growing and dividing cells. Here, we use photoactivated localization microscopy (PALM) to map the cellular locations of three proteins central to bacterial chemotaxis (the Tar receptor, CheY, and CheW) with a precision of 15 nm. We find that cluster sizes are approximately exponentially distributed, with no characteristic cluster size. One-third of Tar receptors are part of smaller lateral clusters and not of the large polar clusters. Analysis of the relative cellular locations of 1.1 million individual proteins (from 326 cells) suggests that clusters form via stochastic self-assembly. The super-resolution PALM maps of E. coli receptors support the notion that stochastic self-assembly can create and maintain approximately periodic structures in biological membranes, without direct cytoskeletal involvement or active transport.},
doi = {10.1371/journal.pbio.1000137},
journal = {PLoS Biology (Online)},
number = 6,
volume = 7,
place = {United States},
year = {Tue Jun 23 00:00:00 EDT 2009},
month = {Tue Jun 23 00:00:00 EDT 2009}
}
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