DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

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 bladdermore » 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.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [2];  [2];  [3] more »;  [3];  [4];  [1] « less
  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)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1265409
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Infection and Immunity
Additional Journal Information:
Journal Volume: 83; Journal Issue: 5; Journal ID: ISSN 0019-9567
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Beatson, Scott A., Ben Zakour, Nouri L., Totsika, Makrina, Forde, Brian M., Watts, Rebecca E., Mabbett, Amanda N., Szubert, Jan M., Sarkar, Sohinee, Phan, Minh-Duy, Peters, Kate M., Petty, Nicola K., Alikhan, Nabil-Fareed, Sullivan, Mitchell J., Gawthorne, Jayde A., Stanton-Cook, Mitchell, Nhu, Nguyen Thi Khanh, Chong, Teik Min, Yin, Wai-Fong, Chan, Kok-Gan, Hancock, Viktoria, Ussery, David W., Ulett, Glen C., and Schembri, Mark A. Molecular Analysis of Asymptomatic Bacteriuria Escherichia coli Strain VR50 Reveals Adaptation to the Urinary Tract by Gene Acquisition. United States: N. p., 2015. Web. doi:10.1128/IAI.02810-14.
Beatson, Scott A., Ben Zakour, Nouri L., Totsika, Makrina, Forde, Brian M., Watts, Rebecca E., Mabbett, Amanda N., Szubert, Jan M., Sarkar, Sohinee, Phan, Minh-Duy, Peters, Kate M., Petty, Nicola K., Alikhan, Nabil-Fareed, Sullivan, Mitchell J., Gawthorne, Jayde A., Stanton-Cook, Mitchell, Nhu, Nguyen Thi Khanh, Chong, Teik Min, Yin, Wai-Fong, Chan, Kok-Gan, Hancock, Viktoria, Ussery, David W., Ulett, Glen C., & Schembri, Mark A. Molecular Analysis of Asymptomatic Bacteriuria Escherichia coli Strain VR50 Reveals Adaptation to the Urinary Tract by Gene Acquisition. United States. https://doi.org/10.1128/IAI.02810-14
Beatson, Scott A., Ben Zakour, Nouri L., Totsika, Makrina, Forde, Brian M., Watts, Rebecca E., Mabbett, Amanda N., Szubert, Jan M., Sarkar, Sohinee, Phan, Minh-Duy, Peters, Kate M., Petty, Nicola K., Alikhan, Nabil-Fareed, Sullivan, Mitchell J., Gawthorne, Jayde A., Stanton-Cook, Mitchell, Nhu, Nguyen Thi Khanh, Chong, Teik Min, Yin, Wai-Fong, Chan, Kok-Gan, Hancock, Viktoria, Ussery, David W., Ulett, Glen C., and Schembri, Mark A. Fri . "Molecular Analysis of Asymptomatic Bacteriuria Escherichia coli Strain VR50 Reveals Adaptation to the Urinary Tract by Gene Acquisition". United States. https://doi.org/10.1128/IAI.02810-14. https://www.osti.gov/servlets/purl/1265409.
@article{osti_1265409,
title = {Molecular Analysis of Asymptomatic Bacteriuria Escherichia coli Strain VR50 Reveals Adaptation to the Urinary Tract by Gene Acquisition},
author = {Beatson, Scott A. and Ben Zakour, Nouri L. and Totsika, Makrina and Forde, Brian M. and Watts, Rebecca E. and Mabbett, Amanda N. and Szubert, Jan M. and Sarkar, Sohinee and Phan, Minh-Duy and Peters, Kate M. and Petty, Nicola K. and Alikhan, Nabil-Fareed and Sullivan, Mitchell J. and Gawthorne, Jayde A. and Stanton-Cook, Mitchell and Nhu, Nguyen Thi Khanh and Chong, Teik Min and Yin, Wai-Fong and Chan, Kok-Gan and Hancock, Viktoria and Ussery, David W. and Ulett, Glen C. and Schembri, Mark A},
abstractNote = {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.},
doi = {10.1128/IAI.02810-14},
journal = {Infection and Immunity},
number = 5,
volume = 83,
place = {United States},
year = {Fri May 01 00:00:00 EDT 2015},
month = {Fri May 01 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 22 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Intramacrophage survival of uropathogenic Escherichia coli: Differences between diverse clinical isolates and between mouse and human macrophages
journal, November 2011


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

  • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
  • Nature Methods, Vol. 10, Issue 6
  • DOI: 10.1038/nmeth.2474

RATT: Rapid Annotation Transfer Tool
journal, February 2011

  • Otto, Thomas D.; Dillon, Gary P.; Degrave, Wim S.
  • Nucleic Acids Research, Vol. 39, Issue 9
  • DOI: 10.1093/nar/gkq1268

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

  • Svanborg, C.; Frendéus, B.; Godaly, G.
  • The Journal of Infectious Diseases, Vol. 183, Issue s1
  • DOI: 10.1086/318858

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

  • Vejborg, Rebecca Munk; Friis, Carsten; Hancock, Viktoria
  • Molecular Genetics and Genomics, Vol. 283, Issue 5
  • DOI: 10.1007/s00438-010-0532-9

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

  • Alikhan, Nabil-Fareed; Petty, Nicola K.; Ben Zakour, Nouri L.
  • BMC Genomics, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2164-12-402

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


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

  • Brzuszkiewicz, E.; Bruggemann, H.; Liesegang, H.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 34
  • DOI: 10.1073/pnas.0603038103

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

  • Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
  • BMC Genomics, Vol. 9, Issue 1, Article No. 75
  • DOI: 10.1186/1471-2164-9-75

SHRiMP2: Sensitive yet Practical Short Read Mapping
journal, January 2011


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

  • Mabbett, A.; Ulett, G.; Watts, R.
  • International Journal of Medical Microbiology, Vol. 299, Issue 1
  • DOI: 10.1016/j.ijmm.2008.06.003

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

  • Watts, Rebecca E.; Totsika, Makrina; Challinor, Victoria L.
  • Infection and Immunity, Vol. 80, Issue 1
  • DOI: 10.1128/iai.05594-11

Molecular Basis of Commensalism in the Urinary Tract: Low Virulence or Virulence Attenuation?
journal, November 2007

  • Zdziarski, Jaroslaw; Svanborg, Catharina; Wullt, Björn
  • Infection and Immunity, Vol. 76, Issue 2
  • DOI: 10.1128/iai.01215-07

UpaG, a New Member of the Trimeric Autotransporter Family of Adhesins in Uropathogenic Escherichia coli
journal, April 2008

  • Valle, Jaione; Mabbett, Amanda N.; Ulett, Glen C.
  • Journal of Bacteriology, Vol. 190, Issue 12
  • DOI: 10.1128/jb.00122-08

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

  • Petty, N. K.; Ben Zakour, N. L.; Stanton-Cook, M.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 15
  • DOI: 10.1073/pnas.1322678111

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


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

  • Cooper, Kerry K.; Mandrell, Robert E.; Louie, Jacqueline W.
  • BMC Genomics, Vol. 15, Issue 1
  • DOI: 10.1186/1471-2164-15-17

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

  • Klemm, Per; Hancock, Viktoria; Schembri, Mark A.
  • Infection and Immunity, Vol. 75, Issue 8
  • DOI: 10.1128/iai.01730-06

Direct detection of DNA methylation during single-molecule, real-time sequencing
journal, May 2010

  • Flusberg, Benjamin A.; Webster, Dale R.; Lee, Jessica H.
  • Nature Methods, Vol. 7, Issue 6
  • DOI: 10.1038/nmeth.1459

Defining Genomic Islands and Uropathogen-Specific Genes in Uropathogenic Escherichia coli
journal, February 2007

  • Lloyd, Amanda L.; Rasko, David A.; Mobley, Harry L. T.
  • Journal of Bacteriology, Vol. 189, Issue 9
  • DOI: 10.1128/jb.01744-06

Reduced Toll‐Like Receptor 4 Expression in Children with Asymptomatic Bacteriuria
journal, August 2007

  • Ragnarsdóttir, Bryndís; Samuelsson, Martin; Gustafsson, Mattias C. U.
  • The Journal of Infectious Diseases, Vol. 196, Issue 3
  • DOI: 10.1086/518893

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

  • Ragnarsdóttir, Bryndís; Lutay, Nataliya; Grönberg-Hernandez, Jenny
  • Nature Reviews Urology, Vol. 8, Issue 8
  • DOI: 10.1038/nrurol.2011.100

Identification of the complement decay-accelerating factor (DAF) on epithelium and glandular cells and in body fluids.
journal, March 1987

  • Medof, M. E.; Walter, E. I.; Rutgers, J. L.
  • Journal of Experimental Medicine, Vol. 165, Issue 3
  • DOI: 10.1084/jem.165.3.848

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


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


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


Using MUMmer to Identify Similar Regions in Large Sequence Sets
journal, January 2003

  • Delcher, Arthur L.; Salzberg, Steven L.; Phillippy, Adam M.
  • Current Protocols in Bioinformatics, Vol. 00, Issue 1
  • DOI: 10.1002/0471250953.bi1003s00

Genomic islands in pathogenic and environmental microorganisms
journal, May 2004

  • Dobrindt, Ulrich; Hochhut, Bianca; Hentschel, Ute
  • Nature Reviews Microbiology, Vol. 2, Issue 5
  • DOI: 10.1038/nrmicro884

progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
journal, June 2010


Ampicillin‐Resistant Escherichia coli in Gestational Pyelonephritis: Increased Occurrence and Association with the Colonization Factor Dr Adhesin
journal, May 2001

  • Hart, Audrey; Nowicki, Bogdan J.; Reisner, Barbara
  • The Journal of Infectious Diseases, Vol. 183, Issue 10
  • DOI: 10.1086/320196

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

  • Braun, Volkmar
  • Frontiers in Bioscience, Vol. 8, Issue 6
  • DOI: 10.2741/1232

Complement Protective Epitopes and CD55–Microtubule Complexes Facilitate the Invasion and Intracellular Persistence of Uropathogenic Escherichia coli
journal, November 2013

  • Rana, Tanu; Hasan, Rafia J.; Nowicki, Stella
  • The Journal of Infectious Diseases, Vol. 209, Issue 7
  • DOI: 10.1093/infdis/jit619

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


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

  • Johnson, Timothy J.; Kariyawasam, Subhashinie; Wannemuehler, Yvonne
  • Journal of Bacteriology, Vol. 189, Issue 8
  • DOI: 10.1128/jb.01726-06

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

  • Korotkova, Natalia; Cota, Ernesto; Lebedin, Yuri
  • Journal of Biological Chemistry, Vol. 281, Issue 39
  • DOI: 10.1074/jbc.m605681200

Uropathogenic Escherichia coli virulence and innate immune responses during urinary tract infection
journal, February 2013

  • Ulett, Glen C.; Totsika, Makrina; Schaale, Kolja
  • Current Opinion in Microbiology, Vol. 16, Issue 1
  • DOI: 10.1016/j.mib.2013.01.005

Dr Fimbriae Operon of Uropathogenic Escherichia coli Mediate Microtubule‐Dependent Invasion to the HeLa Epithelial Cell Line
journal, July 1997

  • Goluszko, Pawel; Popov, Vsevolod; Selvarangan, Rangaraj
  • The Journal of Infectious Diseases, Vol. 176, Issue 1
  • DOI: 10.1086/514018

Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin
journal, July 1998

  • Sokurenko, E. V.; Chesnokova, V.; Dykhuizen, D. E.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 15
  • DOI: 10.1073/pnas.95.15.8922

Asymptomatic bacteriuria Escherichia coli strain 83972 carries mutations in the foc locus and is unable to express F1C fimbriae
journal, June 2006

  • Roos, Viktoria; Schembri, Mark A.; Ulett, Glen C.
  • Microbiology, Vol. 152, Issue 6
  • DOI: 10.1099/mic.0.28711-0

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

  • Datsenko, K. A.; Wanner, B. L.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645
  • DOI: 10.1073/pnas.120163297

ACT: the Artemis comparison tool
journal, June 2005


Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing
journal, December 2011

  • Clark, Tyson A.; Murray, Iain A.; Morgan, Richard D.
  • Nucleic Acids Research, Vol. 40, Issue 4
  • DOI: 10.1093/nar/gkr1146

Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing
journal, November 2012

  • Fang, Gang; Munera, Diana; Friedman, David I.
  • Nature Biotechnology, Vol. 30, Issue 12
  • DOI: 10.1038/nbt.2432

Bacterial control of host gene expression through RNA polymerase II
journal, May 2013

  • Lutay, Nataliya; Ambite, Ines; Hernandez, Jenny Grönberg
  • Journal of Clinical Investigation, Vol. 123, Issue 6
  • DOI: 10.1172/jci66451

Functional Analysis of Antigen 43 in Uropathogenic Escherichia coli Reveals a Role in Long-Term Persistence in the Urinary Tract
journal, April 2007

  • Ulett, Glen C.; Valle, Jaione; Beloin, Christophe
  • Infection and Immunity, Vol. 75, Issue 7
  • DOI: 10.1128/iai.01952-06

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

  • Carver, T.; Harris, S. R.; Otto, T. D.
  • Briefings in Bioinformatics, Vol. 14, Issue 2
  • DOI: 10.1093/bib/bbr073

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

  • Thawai, Chitti; Bunbamrung, Nantiya; Pittayakhajonwut, Pattama
  • Scientific Reports, Vol. 10, Issue 1
  • DOI: 10.1038/s41598-020-68009-y

Urinary Tract Infection Prophylaxis Using Escherichia coli 83972 in Spinal cord Injured Patients
journal, March 2000


Works referencing / citing this record:

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

  • Reitzer, Larry; Zimmern, Philippe
  • Clinical Microbiology Reviews, Vol. 33, Issue 1
  • DOI: 10.1128/cmr.00101-19