The Biology of the Escherichia coli Extracellular Matrix
- Authors: David A. Hufnagel1, William H. Depas2, Matthew R. Chapman3
- Editors: Mahmoud Ghannoum4, Matthew Parsek5, Marvin Whiteley6, Pranab Mukherjee7
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VIEW AFFILIATIONS HIDE AFFILIATIONSAffiliations: 1: Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109; 2: Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109; 3: Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109; 4: Case Western Reserve University, Cleveland, OH; 5: University of Washington, Seattle, WA; 6: University of Texas at Austin, Austin, TX; 7: Case Western Reserve University, Cleveland, OH
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Received 09 September 2014 Accepted 30 September 2014 Published 19 June 2015
- Correspondence: Matthew R. Chapman, [email protected]

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Abstract:
Escherichia coli is one of the world’s best-characterized organisms, because it has been extensively studied for over a century. However, most of this work has focused on E. coli grown under laboratory conditions that do not faithfully simulate its natural environments. Therefore, the historical perspectives on E. coli physiology and life cycle are somewhat skewed toward experimental systems that feature E. coli growing logarithmically in a test tube. Typically a commensal bacterium, E. coli resides in the lower intestines of a slew of animals. Outside of the lower intestine, E. coli can adapt and survive in a very different set of environmental conditions. Biofilm formation allows E. coli to survive, and even thrive, in environments that do not support the growth of planktonic populations. E. coli can form biofilms virtually everywhere: in the bladder during a urinary tract infection, on in-dwelling medical devices, and outside of the host on plants and in the soil. The E. coli extracellular matrix (ECM), primarily composed of the protein polymer named curli and the polysaccharide cellulose, promotes adherence to organic and inorganic surfaces and resistance to desiccation, the host immune system, and other antimicrobials. The pathways that govern E. coli biofilm formation, cellulose production, and curli biogenesis will be discussed in this article, which concludes with insights into the future of E. coli biofilm research and potential therapies.
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Citation: Hufnagel D, Depas W, Chapman M. 2015. The Biology of the Escherichia coli Extracellular Matrix. Microbiol Spectrum 3(3):MB-0014-2014. doi:10.1128/microbiolspec.MB-0014-2014.




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Abstract:
Escherichia coli is one of the world’s best-characterized organisms, because it has been extensively studied for over a century. However, most of this work has focused on E. coli grown under laboratory conditions that do not faithfully simulate its natural environments. Therefore, the historical perspectives on E. coli physiology and life cycle are somewhat skewed toward experimental systems that feature E. coli growing logarithmically in a test tube. Typically a commensal bacterium, E. coli resides in the lower intestines of a slew of animals. Outside of the lower intestine, E. coli can adapt and survive in a very different set of environmental conditions. Biofilm formation allows E. coli to survive, and even thrive, in environments that do not support the growth of planktonic populations. E. coli can form biofilms virtually everywhere: in the bladder during a urinary tract infection, on in-dwelling medical devices, and outside of the host on plants and in the soil. The E. coli extracellular matrix (ECM), primarily composed of the protein polymer named curli and the polysaccharide cellulose, promotes adherence to organic and inorganic surfaces and resistance to desiccation, the host immune system, and other antimicrobials. The pathways that govern E. coli biofilm formation, cellulose production, and curli biogenesis will be discussed in this article, which concludes with insights into the future of E. coli biofilm research and potential therapies.

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Figures

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FIGURE 1
Laboratory E. coli biofilm models. (A) Ring biofilm stained by crystal violet (CV). Cultures were grown in LB media in glass tubes at 26°C for 48 hours. Liquid culture was removed and the tube was stained with 0.1% (w/v) CV for 5 minutes. Tubes were subsequently washed with water. The top image is a WT strain, and the lower image is a flagella mutant (fliC::kan). (B) Pellicle biofilms grown in a 24-well plate for 48 hours at 26°C. Liquid media was removed followed by 5 minutes of staining with 0.1% CV. Stained pellicles were washed three times with water prior to imaging. The top image is a CV-stained WT UTI89 pellicle, whereas the lower picture is a culture of a ΔcsgD mutant that did not produce a pellicle. (C) Pellicle biofilms grown in 1:7500 (Congo red:YESCA) media in a 24-well dish for 48 hours at 26°C. The top image shows a WT UTI89 culture that produced a pellicle, whereas the lower image is a culture of a ΔcsgD mutant that did not form a pellicle. (D) 4-µL spots of 1-OD600 E. coli were grown at 26°C for 48 hours on YESCA CR plates. The colony on the left is UTI89 WT; on the right is a csgD mutant colony.

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FIGURE 2
ECM production model. CsgD is the master regulator of the biofilm extracellular matrix. CsgD transcriptionally upregulates the csgB and csgA genes, which encode the minor and major curli fiber subunits, respectively. CsgA and CsgB are secreted through an outer membrane pore formed by CsgG. CsgE is thought to facilitate translocation of curli subunits across the outer membrane by capping the periplasmic side of the secretion vestibule so that movement in the channel is unidirectional. CsgB associates with the cell surface and templates amyloid polymerization of CsgA. CsgD also transcriptionally upregulates adrA. AdrA is an inner membrane diguanylate cyclase, which produces the secondary messenger, c-di-GMP. c-di-GMP binds and activates BcsA, which then produces cellulose fibers via the building block UDP-glucose. C-di-GMP that activates BcsA can also be produced via YedQ and YfiN.
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