Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy
Citation: Derek Greenfield, Ann L. McEvoy, Hari Shroff, Gavin E. Crooks, Ned S. Wingreen, Eric Betzig, Jan Liphardt (2009/06) Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy. PLoS Biol (Volume 7) (RSS)
DOI (original publisher): 10.1371/journal.pbio.1000137
Semantic Scholar (metadata): 10.1371/journal.pbio.1000137
Sci-Hub (fulltext): 10.1371/journal.pbio.1000137
Internet Archive Scholar (search for fulltext): Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy
Download: http://dx.doi.org/10.1371/journal.pbio.1000137
Tagged: Biology
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Summary
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.
Author Summary
Top Cells arrange their components—proteins, lipids, and nucleic acids—in organized and reproducible ways to optimize the activities of these components and, therefore, to improve cell efficiency and survival. Eukaryotic cells have a complex arrangement of subcellular structures such as membrane-bound organelles and cytoskeletal transport systems. However, subcellular organization is also important in prokaryotic cells, including rod-shaped bacteria such as E. coli, most of which lack such well-developed systems of organelles and motor proteins for transporting cellular cargoes. In fact, it has remained somewhat mysterious how bacteria are able to organize and spatially segregate their interiors. The E. coli chemotaxis network, a system important for the bacterial response to environmental cues, is one of the best-understood biological signal transduction pathways and serves as a useful model for studying bacterial spatial organization because its components display a nonrandom, periodic distribution in mature cells. Chemotaxis receptors aggregate and cluster into large sensory complexes that localize to the poles of bacteria. To understand how these clusters form and what controls their size and density, we use ultrahigh-resolution light microscopy, called photoactivated localization microscopy (PALM), to visualize individual chemoreceptors in single E. coli cells. From these high-resolution images, we determined that receptors are not actively distributed or attached to specific locations in cells. Instead, we show that random receptor diffusion and receptor-receptor interactions are sufficient to generate the observed complex, ordered pattern. This simple mechanism, termed stochastic self-assembly, may prove to be widespread in both prokaryotic and eukaryotic cells.
This was published in an open access journal.
