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Title: Molecular Analysis of Asymptomatic Bacteriuria Escherichia coli Strain VR50 Reveals Adaptation to the Urinary Tract by Gene Acquisition

Journal Article · · Infection and Immunity
DOI:https://doi.org/10.1128/IAI.02810-14· OSTI ID:1265409
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  1. University of Queensland, Brisbane, Queensland (Australia)
  2. University of Malaya, Kuala Lumpur (Malaysia)
  3. Technical Univ. of Denmark, Lyngby (Denmark)
  4. University of Queensland, Brisbane, Queensland (Australia); Griffith University, Gold Coast, Queensland (Australia)
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Urinary tract infections (UTIs) are among the most common infectious diseases of humans, with Escherichia coli for >80% of all cases. One extreme of UTI is asymptomatic bacteriuria (ABU), which occurs as an asymptomatic carrier state that resembles commensalism. Here, 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. In conlusion, our study suggests that E. coli VR50 is a commensal-like strain that has acquired fitness factors that facilitate colonization of the human bladder.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-00OR22725
OSTI ID:
1265409
Journal Information:
Infection and Immunity, Vol. 83, Issue 5; ISSN 0019-9567
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 22 works
Citation information provided by
Web of Science

References (100)

Intramacrophage survival of uropathogenic Escherichia coli: Differences between diverse clinical isolates and between mouse and human macrophages journal November 2011
Characterization of plasmid-borne afa-3 gene clusters encoding afimbrial adhesins expressed by Escherichia coli strains associated with intestinal or urinary tract infections. journal January 1993
Characterization and evidence of mobilization of the LEE pathogenicity island of rabbit-specific strains of enteropathogenic Escherichia coli: LEE pathogenicity island of REPEC journal June 2002
Host–pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection journal May 2012
Epidemiology of urinary tract infections: Incidence, morbidity, and economic costs journal February 2003
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data journal May 2013
RATT: Rapid Annotation Transfer Tool journal February 2011
Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths journal January 2009
Toll‐like Receptor Signaling and Chemokine Receptor Expression Influence the Severity of Urinary Tract Infection journal March 2001
Do type 1 fimbriae promote inflammation in the human urinary tract? journal July 2007
A virulent parent with probiotic progeny: comparative genomics of Escherichia coli strains CFT073, Nissle 1917 and ABU 83972 journal March 2010
Frequency and Organization of pap Homologous DNA in Relation to Clinical Origin of Uropathogenic Escherichia coli journal March 1990
BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons journal August 2011
Transcriptional organization of the F1845 fimbrial adhesin determinant of Escherichia coli journal March 1993
Efficient and accurate whole genome assembly and methylome profiling of E. coli journal January 2013
The afimbrial adhesive sheath encoded by the afa-3 gene cluster of pathogenic Escherichia coli is composed of two adhesins journal February 1996
TLR- and CXCR1-dependent innate immunity: insights into the genetics of urinary tract infections journal October 2008
Trade-Off between Iron Uptake and Protection against Oxidative Stress: Deletion of cueO Promotes Uropathogenic Escherichia coli Virulence in a Mouse Model of Urinary Tract Infection journal August 2008
Universal chemical assay for the detection and determination of siderophores journal January 1987
How to become a uropathogen: Comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains journal August 2006
afa-8 Gene Cluster Is Carried by a Pathogenicity Island Inserted into the tRNAPhe of Human and Bovine Pathogenic Escherichia coli Isolates journal February 2001
The RAST Server: Rapid Annotations using Subsystems Technology journal January 2008
SHRiMP2: Sensitive yet Practical Short Read Mapping journal January 2011
MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium: Regulation of curli and aggregation by mlrA journal July 2001
Role of pathogenicity island-associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536 journal August 2006
Bacterial interference—is deliberate colonization with Escherichia coli 83972 an alternative treatment for patients with recurrent urinary tract infection? journal August 2006
Virulence properties of asymptomatic bacteriuria Escherichia coli journal January 2009
P-fimbriae trigger mucosal responses to Escherichia coli in the human urinary tract journal April 2001
Contribution of Siderophore Systems to Growth and Urinary Tract Colonization of Asymptomatic Bacteriuria Escherichia coli journal September 2011
Molecular Basis of Commensalism in the Urinary Tract: Low Virulence or Virulence Attenuation? journal November 2007
UpaG, a New Member of the Trimeric Autotransporter Family of Adhesins in Uropathogenic Escherichia coli journal April 2008
Virulence Characteristics of Escherichia coli Causing First Urinary Tract Infection Predict Risk of Second Infection journal December 1995
Global dissemination of a multidrug resistant Escherichia coli clone journal March 2014
Analysis of the Genome Structure of the Nonpathogenic Probiotic Escherichia coli Strain Nissle 1917 journal August 2004
Urinary Tract Infection Prophylaxis Using Escherichia coli 83972 in Spinal cord Injured Patients journal March 2000
The Asymptomatic Bacteriuria Escherichia coli Strain 83972 Outcompetes Uropathogenic E. coli Strains in Human Urine journal January 2006
Pathogenesis of Human Diffusely Adhering Escherichia coli Expressing Afa/Dr Adhesins (Afa/Dr DAEC): Current Insights and Future Challenges journal October 2014
Instability of Pathogenicity Islands in Uropathogenic Escherichia coli 536 journal May 2004
Uropathogenic Escherichia coli Mediated Urinary Tract Infection journal August 2012
Comparative genomics of enterohemorrhagic Escherichia coli O145:H28 demonstrates a common evolutionary lineage with Escherichia coli O157:H7 journal January 2014
Genetic Control of the Variable Innate Immune Response to Asymptomatic Bacteriuria journal November 2011
Mellowing Out: Adaptation to Commensalism by Escherichia coli Asymptomatic Bacteriuria Strain 83972 journal May 2007
Direct detection of DNA methylation during single-molecule, real-time sequencing journal May 2010
Defining Genomic Islands and Uropathogen-Specific Genes in Uropathogenic Escherichia coli journal February 2007
Reduced Toll‐Like Receptor 4 Expression in Children with Asymptomatic Bacteriuria
  • Ragnarsdóttir, Bryndís; Samuelsson, Martin; Gustafsson, Mattias C. U.
  • The Journal of Infectious Diseases, Vol. 196, Issue 3 https://doi.org/10.1086/518893
journal August 2007
Molecular cloning and characterization of Dr-II, a nonfimbrial adhesin-I-like adhesin isolated from gestational pyelonephritis-associated Escherichia coli that binds to decay-accelerating factor. journal January 1997
Molecular Characterization of the Escherichia coli Asymptomatic Bacteriuria Strain 83972: the Taming of a Pathogen journal January 2006
Pathogenicity Islands and the Evolution of Microbes journal October 2000
Genetics of innate immunity and UTI susceptibility journal July 2011
Genetic organization of the afimbrial adhesin operon and nucleotide sequence from a uropathogenic Escherichia coli gene encoding an afimbrial adhesin. journal January 1985
Identification of the complement decay-accelerating factor (DAF) on epithelium and glandular cells and in body fluids. journal March 1987
Adhesion, hemagglutination, and virulence of Escherichia coli causing urinary tract infections. journal January 1981
Molecular cloning of the Escherichia coli O75X adhesin. journal January 1987
Global Gene Expression Profiling of the Asymptomatic Bacteriuria Escherichia coli Strain 83972 in the Human Urinary Tract journal June 2006
Short consensus repeat-3 domain of recombinant decay-accelerating factor is recognized by Escherichia coli recombinant Dr adhesin in a model of a cell-cell interaction. journal December 1993
Host Imprints on Bacterial Genomes—Rapid, Divergent Evolution in Individual Patients journal August 2010
Epidemiology of urinary tract infections: incidence, morbidity, and economic costs journal July 2002
Dissemination of pheU- and pheV-located genomic islands among enteropathogenic (EPEC) and enterohemorrhagic (EHEC) E. coli and their possible role in the horizontal transfer of the locus of enterocyte effacement (LEE) journal January 2003
A novel locus of enterocyte effacement (LEE) pathogenicity island inserted at phe V in bovine Shiga toxin-producing Escherichia coli strain O103:H2 journal October 2001
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models journal August 2006
Molecular Cloning and Characterization of the afa-7and afa-8 Gene Clusters Encoding Afimbrial Adhesins inEscherichia coli Strains Associated with Diarrhea or Septicemia in Calves journal October 1999
Using MUMmer to Identify Similar Regions in Large Sequence Sets journal January 2003
Genomic islands in pathogenic and environmental microorganisms journal May 2004
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement journal June 2010
Differential recognition of members of the carcinoembryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC): CEACAM receptors for Afa/Dr adhesins journal April 2004
Ampicillin‐Resistant Escherichia coli in Gestational Pyelonephritis: Increased Occurrence and Association with the Colonization Factor Dr Adhesin journal May 2001
Toll-Like Receptor 4 Promoter Polymorphisms: Common TLR4 Variants May Protect against Severe Urinary Tract Infection journal May 2010
Iron uptake by em Escherichia Coli em journal January 2003
Complement Protective Epitopes and CD55–Microtubule Complexes Facilitate the Invasion and Intracellular Persistence of Uropathogenic Escherichia coli journal November 2013
Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood group-independent, mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. journal January 1984
Selection for functional diversity drives accumulation of point mutations in Dr adhesins of Escherichia coli: Functional diversity in E. coli Dr adhesins journal March 2007
Comparison of Asymptomatic Bacteriuria Escherichia coli Isolates from Healthy Individuals versus Those from Hospital Patients Shows that Long-Term Bladder Colonization Selects for Attenuated Virulence Phenotypes journal November 2011
The Genome Sequence of Avian Pathogenic Escherichia coli Strain O1:K1:H7 Shares Strong Similarities with Human Extraintestinal Pathogenic E. coli Genomes journal February 2007
Asymptomatic bacteriuria Escherichia coli strains: adhesins, growth and competition journal September 2006
A Subfamily of Dr Adhesins of Escherichia coli Bind Independently to Decay-accelerating Factor and the N-domain of Carcinoembryonic Antigen journal August 2006
Uropathogenic Escherichia coli virulence and innate immune responses during urinary tract infection journal February 2013
Dr Fimbriae Operon of Uropathogenic Escherichia coli Mediate Microtubule‐Dependent Invasion to the HeLa Epithelial Cell Line journal July 1997
Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin journal July 1998
Asymptomatic bacteriuria Escherichia coli strain 83972 carries mutations in the foc locus and is unable to express F1C fimbriae journal June 2006
Persistence of Escherichia coli bacteriuria is not determined by bacterial adherence. journal January 1991
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products journal May 2000
ACT: the Artemis comparison tool journal June 2005
Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing journal December 2011
Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing journal November 2012
Bacterial control of host gene expression through RNA polymerase II journal May 2013
Functional Analysis of Antigen 43 in Uropathogenic Escherichia coli Reveals a Role in Long-Term Persistence in the Urinary Tract journal April 2007
Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. journal January 1989
Development of experimental model of chronic pyelonephritis with Escherichia coli O75:K5:H-bearing Dr fimbriae: mutation in the dra region prevented tubulointerstitial nephritis. journal April 1997
Bacterial adhesins: function and structure journal March 2000
Pathogenesis of Afa/Dr Diffusely Adhering Escherichia coli journal April 2005
BamView: visualizing and interpretation of next-generation sequencing read alignments journal January 2012
Analysis of Genome Plasticity in Pathogenic and Commensal Escherichia coli Isolates by Use of DNA Arrays journal March 2003
Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. journal January 1990
Rapid and Simple Determination of theEscherichia coli Phylogenetic Group journal October 2000
Iron acquisition in plague: modular logic in enzymatic biogenesis of yersiniabactin by Yersinia pestis journal October 1998
TonB-Dependent Systems of Uropathogenic Escherichia coli: Aerobactin and Heme Transport and TonB Are Required for Virulence in the Mouse journal October 2001
Integrating whole-genome sequencing within the National Antimicrobial Resistance Surveillance Program in the Philippines journal June 2020
A novel diterpene agent isolated from Microbispora hainanensis strain CSR-4 and its in vitro and in silico inhibition effects on acetylcholine esterase enzyme journal July 2020
Urinary Tract Infection Prophylaxis Using Escherichia coli 83972 in Spinal cord Injured Patients journal March 2000
afa-8 Gene Cluster Is Carried by a Pathogenicity Island Inserted into the tRNA Phe of Human and Bovine Pathogenic Escherichia coli Isolates journal June 2002

Cited By (3)

A clinical approach to multidrug-resistant urinary tract infection and subclinical bacteriuria in dogs and cats journal November 2019
Whole-genome sequencing in the prediction of antimicrobial resistance journal June 2016
Rapid Growth and Metabolism of Uropathogenic Escherichia coli in Relation to Urine Composition journal October 2019

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