Evolutionary adaptation of an AraC-like regulatory protein in Citrobacter rodentium and Escherichia species

Tan, A; Petty, NK; Hocking, D; Bennett-Wood, V; Wakefield, M; Praszkier, J; Tauschek, M; Yang, J; Robins-Browne, R

Evolutionary adaptation of an AraC-like regulatory protein in Citrobacter rodentium and Escherichia species

Tan, A Petty, NK

Hocking, D Bennett-Wood, V Wakefield, M Praszkier, J Tauschek, M Yang, J Robins-Browne, R

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Publication Type:: Journal Article
Citation:: Infection and Immunity, 2015, 83 (4), pp. 1384 - 1395
Issue Date:: 2015-01-01

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Field	Value	Language
dc.contributor.author	Tan, A	en_US
dc.contributor.author	Petty, NK https://orcid.org/0000-0001-6528-9886	en_US
dc.contributor.author	Hocking, D	en_US
dc.contributor.author	Bennett-Wood, V	en_US
dc.contributor.author	Wakefield, M	en_US
dc.contributor.author	Praszkier, J	en_US
dc.contributor.author	Tauschek, M	en_US
dc.contributor.author	Yang, J	en_US
dc.contributor.author	Robins-Browne, R	en_US
dc.date.issued	2015-01-01	en_US
dc.identifier.citation	Infection and Immunity, 2015, 83 (4), pp. 1384 - 1395	en_US
dc.identifier.issn	0019-9567	en_US
dc.identifier.uri	http://hdl.handle.net/10453/116066
dc.description.abstract	© 2015, American Society for Microbiology. The evolution of pathogenic bacteria is a multifaceted and complex process, which is strongly influenced by the horizontal acquisition of genetic elements and their subsequent expression in their new hosts. A well-studied example is the RegA regulon of the enteric pathogen Citrobacter rodentium. The RegA regulatory protein is a member of the AraC/XylS superfamily, which coordinates the expression of a gene repertoire that is necessary for full pathogenicity of this murine pathogen. Upon stimulation by an exogenous, gut-associated signal, namely, bicarbonate ions, RegA activates the expression of a series of genes, including virulence factors, such as autotransporters, fimbriae, a dispersin-like protein, and the grlRA operon on the locus of enterocyte effacement pathogenicity island. Interestingly, the genes encoding RegA homologues are distributed across the genus Escherichia, encompassing pathogenic and nonpathogenic subtypes. In this study, we carried out a series of bioinformatic, transcriptional, and functional analyses of the RegA regulons of these bacteria. Our results demonstrated that regA has been horizontally transferred to Escherichia spp. and C. rodentium. Comparative studies of two RegA homologues, namely, those from C. rodentium and E. coli SMS-3-5, a multiresistant environmental strain of E. coli, showed that the two regulators acted similarly in vitro but differed in terms of their abilities to activate the virulence of C. rodentium in vivo, which evidently was due to their differential activation of grlRA. Our data indicate that RegA from C. rodentium has strain-specific adaptations that facilitate infection of its murine host. These findings shed new light on the development of virulence by C. rodentium and on the evolution of virulence- regulatory genes of bacterial pathogens in general.	en_US
dc.relation.ispartof	Infection and Immunity	en_US
dc.relation.isbasedon	10.1128/IAI.02697-14	en_US
dc.subject.classification	Microbiology	en_US
dc.subject.mesh	Animals	en_US
dc.subject.mesh	Mice, Inbred C57BL	en_US
dc.subject.mesh	Mice	en_US
dc.subject.mesh	Citrobacter rodentium	en_US
dc.subject.mesh	Escherichia coli	en_US
dc.subject.mesh	Bacterial Proteins	en_US
dc.subject.mesh	Escherichia coli Proteins	en_US
dc.subject.mesh	Phosphoproteins	en_US
dc.subject.mesh	Repressor Proteins	en_US
dc.subject.mesh	Virulence Factors	en_US
dc.subject.mesh	Phylogeny	en_US
dc.subject.mesh	Gene Expression Regulation, Bacterial	en_US
dc.subject.mesh	Gene Transfer, Horizontal	en_US
dc.subject.mesh	Male	en_US
dc.subject.mesh	AraC Transcription Factor	en_US
dc.subject.mesh	Biological Evolution	en_US
dc.title	Evolutionary adaptation of an AraC-like regulatory protein in Citrobacter rodentium and Escherichia species	en_US
dc.type	Journal Article
utslib.citation.volume	4	en_US
utslib.citation.volume	83	en_US
utslib.for	110309 Infectious Diseases	en_US
utslib.for	110801 Medical Bacteriology	en_US
utslib.for	060501 Bacteriology	en_US
utslib.for	06 Biological Sciences	en_US
utslib.for	07 Agricultural and Veterinary Sciences	en_US
utslib.for	11 Medical and Health Sciences	en_US
pubs.embargo.period	Not known	en_US
pubs.organisational-group	/University of Technology Sydney
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Strength - ithree - Institute of Infection, Immunity and Innovation
utslib.copyright.status	open_access
pubs.issue	4	en_US
pubs.publication-status	Published	en_US
pubs.volume	83	en_US

Abstract:

© 2015, American Society for Microbiology. The evolution of pathogenic bacteria is a multifaceted and complex process, which is strongly influenced by the horizontal acquisition of genetic elements and their subsequent expression in their new hosts. A well-studied example is the RegA regulon of the enteric pathogen Citrobacter rodentium. The RegA regulatory protein is a member of the AraC/XylS superfamily, which coordinates the expression of a gene repertoire that is necessary for full pathogenicity of this murine pathogen. Upon stimulation by an exogenous, gut-associated signal, namely, bicarbonate ions, RegA activates the expression of a series of genes, including virulence factors, such as autotransporters, fimbriae, a dispersin-like protein, and the grlRA operon on the locus of enterocyte effacement pathogenicity island. Interestingly, the genes encoding RegA homologues are distributed across the genus Escherichia, encompassing pathogenic and nonpathogenic subtypes. In this study, we carried out a series of bioinformatic, transcriptional, and functional analyses of the RegA regulons of these bacteria. Our results demonstrated that regA has been horizontally transferred to Escherichia spp. and C. rodentium. Comparative studies of two RegA homologues, namely, those from C. rodentium and E. coli SMS-3-5, a multiresistant environmental strain of E. coli, showed that the two regulators acted similarly in vitro but differed in terms of their abilities to activate the virulence of C. rodentium in vivo, which evidently was due to their differential activation of grlRA. Our data indicate that RegA from C. rodentium has strain-specific adaptations that facilitate infection of its murine host. These findings shed new light on the development of virulence by C. rodentium and on the evolution of virulence- regulatory genes of bacterial pathogens in general.

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http://hdl.handle.net/10453/116066