Molecular analysis of asymptomatic bacteriuria Escherichia coli strain VR50 reveals adaptation to the urinary tract by gene acquisition

Beatson, SA; Ben Zakour, NL; Totsika, M; Forde, BM; Watts, RE; Mabbett, AN; Szubert, JM; Sarkar, S; Phan, MD; Peters, KM; Petty, NK; Alikhan, NF; Sullivan, MJ; Gawthorne, JA; Stanton-Cook, M; Nhu, NTK; Chong, TM; Yin, WF; Chan, KG; Hancock, V; Ussery, DW; Ulett, GC; Schembri, MA

Molecular analysis of asymptomatic bacteriuria Escherichia coli strain VR50 reveals adaptation to the urinary tract by gene acquisition

Beatson, SA Ben Zakour, NL Totsika, M Forde, BM Watts, RE Mabbett, AN Szubert, JM Sarkar, S Phan, MD Peters, KM Petty, NK

Alikhan, NF Sullivan, MJ Gawthorne, JA Stanton-Cook, M Nhu, NTK Chong, TM Yin, WF Chan, KG Hancock, V Ussery, DW Ulett, GC Schembri, MA

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Publication Type:: Journal Article
Citation:: Infection and Immunity, 2015, 83 (5), pp. 1749 - 1764
Issue Date:: 2015-01-01

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Field	Value	Language
dc.contributor.author	Beatson, SA	en_US
dc.contributor.author	Ben Zakour, NL	en_US
dc.contributor.author	Totsika, M	en_US
dc.contributor.author	Forde, BM	en_US
dc.contributor.author	Watts, RE	en_US
dc.contributor.author	Mabbett, AN	en_US
dc.contributor.author	Szubert, JM	en_US
dc.contributor.author	Sarkar, S	en_US
dc.contributor.author	Phan, MD	en_US
dc.contributor.author	Peters, KM	en_US
dc.contributor.author	Petty, NK https://orcid.org/0000-0001-6528-9886	en_US
dc.contributor.author	Alikhan, NF	en_US
dc.contributor.author	Sullivan, MJ	en_US
dc.contributor.author	Gawthorne, JA	en_US
dc.contributor.author	Stanton-Cook, M	en_US
dc.contributor.author	Nhu, NTK	en_US
dc.contributor.author	Chong, TM	en_US
dc.contributor.author	Yin, WF	en_US
dc.contributor.author	Chan, KG	en_US
dc.contributor.author	Hancock, V	en_US
dc.contributor.author	Ussery, DW	en_US
dc.contributor.author	Ulett, GC	en_US
dc.contributor.author	Schembri, MA	en_US
dc.date.available	2015-01-09	en_US
dc.date.issued	2015-01-01	en_US
dc.identifier.citation	Infection and Immunity, 2015, 83 (5), pp. 1749 - 1764	en_US
dc.identifier.issn	0019-9567	en_US
dc.identifier.uri	http://hdl.handle.net/10453/116063
dc.description.abstract	© 2015, American Society for Microbiology. Urinary tract infections (UTIs) are among the most common infectious diseases of humans, with Escherichia coli responsible for >80% of all cases. One extreme of UTI is asymptomatic bacteriuria (ABU), which occurs as an asymptomatic carrier state that resembles commensalism. To understand the evolution and molecular mechanisms that underpin ABU, the genome of the ABU E. coli strain VR50 was sequenced. Analysis of the complete genome indicated that it most resembles E. coli K-12, with the addition of a 94-kb genomic island (GI-VR50-pheV), eight prophages, and multiple plasmids. GI-VR50-pheV has a mosaic structure and contains genes encoding a number of UTI-associated virulence factors, namely, Afa (afimbrial adhesin), two autotransporter proteins (Ag43 and Sat), and aerobactin. We demonstrated that the presence of this island in VR50 confers its ability to colonize the murine bladder, as a VR50 mutant with GI-VR50-pheV deleted was attenuated in a mouse model of UTI in vivo.We established that Afa is the island-encoded factor responsible for this phenotype using two independent deletion (Afa operon and AfaE adhesin) mutants. E. coli VR50afa and VR50afaE displayed significantly decreased ability to adhere to human bladder epithelial cells. In the mouse model of UTI, VR50afa and VR50afaE displayed reduced bladder colonization compared to wild-type VR50, similar to the colonization level of the GI-VR50-pheV mutant. Our study suggests that E. coli VR50 is a commensal-like strain that has acquired fitness factors that facilitate colonization of the human bladder.	en_US
dc.relation.ispartof	Infection and Immunity	en_US
dc.relation.isbasedon	10.1128/IAI.02810-14	en_US
dc.subject.classification	Microbiology	en_US
dc.subject.mesh	Urinary Tract	en_US
dc.subject.mesh	Cell Line	en_US
dc.subject.mesh	Epithelial Cells	en_US
dc.subject.mesh	Animals	en_US
dc.subject.mesh	Mice, Inbred C57BL	en_US
dc.subject.mesh	Humans	en_US
dc.subject.mesh	Escherichia coli	en_US
dc.subject.mesh	Escherichia coli Infections	en_US
dc.subject.mesh	Bacteriuria	en_US
dc.subject.mesh	DNA, Bacterial	en_US
dc.subject.mesh	Sequence Analysis, DNA	en_US
dc.subject.mesh	Models, Animal	en_US
dc.subject.mesh	Carrier State	en_US
dc.subject.mesh	Adaptation, Biological	en_US
dc.subject.mesh	Evolution, Molecular	en_US
dc.subject.mesh	Bacterial Adhesion	en_US
dc.subject.mesh	Genome, Bacterial	en_US
dc.subject.mesh	Molecular Sequence Data	en_US
dc.subject.mesh	Adult	en_US
dc.subject.mesh	Female	en_US
dc.title	Molecular analysis of asymptomatic bacteriuria Escherichia coli strain VR50 reveals adaptation to the urinary tract by gene acquisition	en_US
dc.type	Journal Article
utslib.citation.volume	5	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	5	en_US
pubs.publication-status	Published	en_US
pubs.volume	83	en_US

Abstract:

© 2015, American Society for Microbiology. Urinary tract infections (UTIs) are among the most common infectious diseases of humans, with Escherichia coli responsible for >80% of all cases. One extreme of UTI is asymptomatic bacteriuria (ABU), which occurs as an asymptomatic carrier state that resembles commensalism. To understand the evolution and molecular mechanisms that underpin ABU, the genome of the ABU E. coli strain VR50 was sequenced. Analysis of the complete genome indicated that it most resembles E. coli K-12, with the addition of a 94-kb genomic island (GI-VR50-pheV), eight prophages, and multiple plasmids. GI-VR50-pheV has a mosaic structure and contains genes encoding a number of UTI-associated virulence factors, namely, Afa (afimbrial adhesin), two autotransporter proteins (Ag43 and Sat), and aerobactin. We demonstrated that the presence of this island in VR50 confers its ability to colonize the murine bladder, as a VR50 mutant with GI-VR50-pheV deleted was attenuated in a mouse model of UTI in vivo.We established that Afa is the island-encoded factor responsible for this phenotype using two independent deletion (Afa operon and AfaE adhesin) mutants. E. coli VR50afa and VR50afaE displayed significantly decreased ability to adhere to human bladder epithelial cells. In the mouse model of UTI, VR50afa and VR50afaE displayed reduced bladder colonization compared to wild-type VR50, similar to the colonization level of the GI-VR50-pheV mutant. Our study suggests that E. coli VR50 is a commensal-like strain that has acquired fitness factors that facilitate colonization of the human bladder.

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http://hdl.handle.net/10453/116063