Radial and Spiral Stream Formation in Proteus mirabilis Colonies

The enteric bacterium Proteus mirabilis, which is a pathogen that forms biofilms in vivo, can swarm over hard surfaces and form a variety of spatial patterns in colonies. Colony formation involves two distinct cell types: swarmer cells that dominate near the surface and the leading edge, and swimmer...

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Main Authors: Xue, Chuan, Othmer, Hans G., Budrene-Kac, Elena O.
Other Authors: Massachusetts Institute of Technology. Department of Mathematics
Format: Article
Language:en_US
Published: Public Library of Science 2012
Online Access:http://hdl.handle.net/1721.1/69175
https://orcid.org/0000-0002-5682-6595
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author Xue, Chuan
Othmer, Hans G.
Budrene-Kac, Elena O.
author2 Massachusetts Institute of Technology. Department of Mathematics
author_facet Massachusetts Institute of Technology. Department of Mathematics
Xue, Chuan
Othmer, Hans G.
Budrene-Kac, Elena O.
author_sort Xue, Chuan
collection MIT
description The enteric bacterium Proteus mirabilis, which is a pathogen that forms biofilms in vivo, can swarm over hard surfaces and form a variety of spatial patterns in colonies. Colony formation involves two distinct cell types: swarmer cells that dominate near the surface and the leading edge, and swimmer cells that prefer a less viscous medium, but the mechanisms underlying pattern formation are not understood. New experimental investigations reported here show that swimmer cells in the center of the colony stream inward toward the inoculation site and in the process form many complex patterns, including radial and spiral streams, in addition to previously-reported concentric rings. These new observations suggest that swimmers are motile and that indirect interactions between them are essential in the pattern formation. To explain these observations we develop a hybrid model comprising cell-based and continuum components that incorporates a chemotactic response of swimmers to a chemical they produce. The model predicts that formation of radial streams can be explained as the modulation of the local attractant concentration by the cells, and that the chirality of the spiral streams results from a swimming bias of the cells near the surface of the substrate. The spatial patterns generated from the model are in qualitative agreement with the experimental observations.
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spelling mit-1721.1/691752022-09-27T17:36:38Z Radial and Spiral Stream Formation in Proteus mirabilis Colonies Xue, Chuan Othmer, Hans G. Budrene-Kac, Elena O. Massachusetts Institute of Technology. Department of Mathematics Budrene-Kac, Elena O. Budrene-Kac, Elena O. The enteric bacterium Proteus mirabilis, which is a pathogen that forms biofilms in vivo, can swarm over hard surfaces and form a variety of spatial patterns in colonies. Colony formation involves two distinct cell types: swarmer cells that dominate near the surface and the leading edge, and swimmer cells that prefer a less viscous medium, but the mechanisms underlying pattern formation are not understood. New experimental investigations reported here show that swimmer cells in the center of the colony stream inward toward the inoculation site and in the process form many complex patterns, including radial and spiral streams, in addition to previously-reported concentric rings. These new observations suggest that swimmers are motile and that indirect interactions between them are essential in the pattern formation. To explain these observations we develop a hybrid model comprising cell-based and continuum components that incorporates a chemotactic response of swimmers to a chemical they produce. The model predicts that formation of radial streams can be explained as the modulation of the local attractant concentration by the cells, and that the chirality of the spiral streams results from a swimming bias of the cells near the surface of the substrate. The spatial patterns generated from the model are in qualitative agreement with the experimental observations. Ohio State University (start-up grant) National Science Foundation (U.S.) (Grant DMS 0817529) University of Minnesota Supercomputing Institute Mathematical Biosciences Institute at the Ohio State University National Science Foundation (U.S.) (Grant DMS 0931642) 2012-02-23T19:19:25Z 2012-02-23T19:19:25Z 2011-12 2011-03 Article http://purl.org/eprint/type/JournalArticle 1553-734X 1553-7358 http://hdl.handle.net/1721.1/69175 Xue, Chuan, Elena O. Budrene, and Hans G. Othmer. “Radial and Spiral Stream Formation in Proteus Mirabilis Colonies.” Ed. Oskar Hallatschek. PLoS Computational Biology 7.12 (2011): e1002332. Web. 23 Feb. 2012. https://orcid.org/0000-0002-5682-6595 en_US http://dx.doi.org/10.1371/journal.pcbi.1002332 PLoS Computational Biology Creative Commons Attribution http://creativecommons.org/licenses/by/2.5/ application/pdf Public Library of Science PLoS
spellingShingle Xue, Chuan
Othmer, Hans G.
Budrene-Kac, Elena O.
Radial and Spiral Stream Formation in Proteus mirabilis Colonies
title Radial and Spiral Stream Formation in Proteus mirabilis Colonies
title_full Radial and Spiral Stream Formation in Proteus mirabilis Colonies
title_fullStr Radial and Spiral Stream Formation in Proteus mirabilis Colonies
title_full_unstemmed Radial and Spiral Stream Formation in Proteus mirabilis Colonies
title_short Radial and Spiral Stream Formation in Proteus mirabilis Colonies
title_sort radial and spiral stream formation in proteus mirabilis colonies
url http://hdl.handle.net/1721.1/69175
https://orcid.org/0000-0002-5682-6595
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