The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli
Curli amyloid fibers are the major protein component of the extracellular matrix produced by Enterobacteriaceae during biofilm formation. Curli are required for proper biofilm development and environmental persistence by Escherichia coli. Here, we present a complete and vetted genetic analysis of fu...
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doaj-6d63b3d4925f44ea8a37e3d20b2dbcfa2020-11-24T22:01:25ZengMDPI AGBiomolecules2218-273X2017-10-01747510.3390/biom7040075biom7040075The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coliDaniel R. Smith0Janet E. Price1Peter E. Burby2Luz P. Blanco3Justin Chamberlain4Matthew R. Chapman5Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USADepartment of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USADepartment of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USADepartment of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USADepartment of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USADepartment of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USACurli amyloid fibers are the major protein component of the extracellular matrix produced by Enterobacteriaceae during biofilm formation. Curli are required for proper biofilm development and environmental persistence by Escherichia coli. Here, we present a complete and vetted genetic analysis of functional amyloid fiber biogenesis. The Keio collection of single gene deletions was screened on Congo red indicator plates to identify E. coli mutants that had defective amyloid production. We discovered that more than three hundred gene products modulated curli production. These genes were involved in fundamental cellular processes such as regulation, environmental sensing, respiration, metabolism, cell envelope biogenesis, transport, and protein turnover. The alternative sigma factors, σS and σE, had opposing roles in curli production. Mutations that induced the σE or Cpx stress response systems had reduced curli production, while mutant strains with increased σS levels had increased curli production. Mutations in metabolic pathways, including gluconeogenesis and the biosynthesis of lipopolysaccharide (LPS), produced less curli. Regulation of the master biofilm regulator, CsgD, was diverse, and the screen revealed several proteins and small RNAs (sRNA) that regulate csgD messenger RNA (mRNA) levels. Using previously published studies, we found minimal overlap between the genes affecting curli biogenesis and genes known to impact swimming or swarming motility, underlying the distinction between motile and sessile lifestyles. Collectively, the diversity and number of elements required suggest curli production is part of a highly regulated and complex developmental pathway in E. coli.https://www.mdpi.com/2218-273X/7/4/75amyloidcurliKeio collectioncsgAcsgDLPSRpoSRpoEEscherichia colinhaArafF |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Daniel R. Smith Janet E. Price Peter E. Burby Luz P. Blanco Justin Chamberlain Matthew R. Chapman |
spellingShingle |
Daniel R. Smith Janet E. Price Peter E. Burby Luz P. Blanco Justin Chamberlain Matthew R. Chapman The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli Biomolecules amyloid curli Keio collection csgA csgD LPS RpoS RpoE Escherichia coli nhaA rafF |
author_facet |
Daniel R. Smith Janet E. Price Peter E. Burby Luz P. Blanco Justin Chamberlain Matthew R. Chapman |
author_sort |
Daniel R. Smith |
title |
The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli |
title_short |
The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli |
title_full |
The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli |
title_fullStr |
The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli |
title_full_unstemmed |
The Production of Curli Amyloid Fibers Is Deeply Integrated into the Biology of Escherichia coli |
title_sort |
production of curli amyloid fibers is deeply integrated into the biology of escherichia coli |
publisher |
MDPI AG |
series |
Biomolecules |
issn |
2218-273X |
publishDate |
2017-10-01 |
description |
Curli amyloid fibers are the major protein component of the extracellular matrix produced by Enterobacteriaceae during biofilm formation. Curli are required for proper biofilm development and environmental persistence by Escherichia coli. Here, we present a complete and vetted genetic analysis of functional amyloid fiber biogenesis. The Keio collection of single gene deletions was screened on Congo red indicator plates to identify E. coli mutants that had defective amyloid production. We discovered that more than three hundred gene products modulated curli production. These genes were involved in fundamental cellular processes such as regulation, environmental sensing, respiration, metabolism, cell envelope biogenesis, transport, and protein turnover. The alternative sigma factors, σS and σE, had opposing roles in curli production. Mutations that induced the σE or Cpx stress response systems had reduced curli production, while mutant strains with increased σS levels had increased curli production. Mutations in metabolic pathways, including gluconeogenesis and the biosynthesis of lipopolysaccharide (LPS), produced less curli. Regulation of the master biofilm regulator, CsgD, was diverse, and the screen revealed several proteins and small RNAs (sRNA) that regulate csgD messenger RNA (mRNA) levels. Using previously published studies, we found minimal overlap between the genes affecting curli biogenesis and genes known to impact swimming or swarming motility, underlying the distinction between motile and sessile lifestyles. Collectively, the diversity and number of elements required suggest curli production is part of a highly regulated and complex developmental pathway in E. coli. |
topic |
amyloid curli Keio collection csgA csgD LPS RpoS RpoE Escherichia coli nhaA rafF |
url |
https://www.mdpi.com/2218-273X/7/4/75 |
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