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

Title: Comparative Genomics Applied to Systematically Assess Pathogenicity Potential in Shiga Toxin-Producing Escherichia coli O145:H28

Abstract

Shiga toxin-producing Escherichia coli (STEC) O145:H28 can cause severe disease in humans and is a predominant serotype in STEC O145 environmental isolates. Here, comparative genomics was applied to a set of clinical and environmental strains to systematically evaluate the pathogenicity potential in environmental strains. While the core genes-based tree separated all O145:H28 strains from the non O145:H28 reference strains, it failed to segregate environmental strains from the clinical. In contrast, the accessory genes-based tree placed all clinical strains in the same clade regardless of their genotypes or serotypes, apart from the environmental strains. Loss-of-function mutations were common in the virulence genes examined, with a high frequency in genes related to adherence, autotransporters, and the type three secretion system. Distinct differences in pathogenicity islands LEE, OI-122, and OI-57, the acid fitness island, and the tellurite resistance island were detected between the O145:H28 and reference strains. A great amount of genetic variation was detected in O145:H28, which was mainly attributed to deletions, insertions, and gene acquisition at several chromosomal “hot spots”. Finally, our study demonstrated a distinct virulence gene repertoire among the STEC O145:H28 strains originating from the same geographical region and revealed unforeseen contributions of loss-of-function mutations to virulence evolution andmore » genetic diversification in STEC.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [2]
  1. US Dept. of Agriculture (USDA), Albany, CA (United States). Western Regional Research Center
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDA; USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1968211
Report Number(s):
LA-UR-23-23078
Journal ID: ISSN 2076-2607
Grant/Contract Number:  
89233218CNA000001
Resource Type:
Accepted Manuscript
Journal Name:
Microorganisms
Additional Journal Information:
Journal Volume: 10; Journal Issue: 5; Journal ID: ISSN 2076-2607
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biological science; Shiga toxin-producing Escherichia coli (STEC); pangenome; pathogenicity islands; virulence genes

Citation Formats

Carter, Michelle Qiu, Laniohan, Nicole, Lo, Chien-Chi, and Chain, Patrick G. Comparative Genomics Applied to Systematically Assess Pathogenicity Potential in Shiga Toxin-Producing Escherichia coli O145:H28. United States: N. p., 2022. Web. doi:10.3390/microorganisms10050866.
Carter, Michelle Qiu, Laniohan, Nicole, Lo, Chien-Chi, & Chain, Patrick G. Comparative Genomics Applied to Systematically Assess Pathogenicity Potential in Shiga Toxin-Producing Escherichia coli O145:H28. United States. https://doi.org/10.3390/microorganisms10050866
Carter, Michelle Qiu, Laniohan, Nicole, Lo, Chien-Chi, and Chain, Patrick G. Thu . "Comparative Genomics Applied to Systematically Assess Pathogenicity Potential in Shiga Toxin-Producing Escherichia coli O145:H28". United States. https://doi.org/10.3390/microorganisms10050866. https://www.osti.gov/servlets/purl/1968211.
@article{osti_1968211,
title = {Comparative Genomics Applied to Systematically Assess Pathogenicity Potential in Shiga Toxin-Producing Escherichia coli O145:H28},
author = {Carter, Michelle Qiu and Laniohan, Nicole and Lo, Chien-Chi and Chain, Patrick G.},
abstractNote = {Shiga toxin-producing Escherichia coli (STEC) O145:H28 can cause severe disease in humans and is a predominant serotype in STEC O145 environmental isolates. Here, comparative genomics was applied to a set of clinical and environmental strains to systematically evaluate the pathogenicity potential in environmental strains. While the core genes-based tree separated all O145:H28 strains from the non O145:H28 reference strains, it failed to segregate environmental strains from the clinical. In contrast, the accessory genes-based tree placed all clinical strains in the same clade regardless of their genotypes or serotypes, apart from the environmental strains. Loss-of-function mutations were common in the virulence genes examined, with a high frequency in genes related to adherence, autotransporters, and the type three secretion system. Distinct differences in pathogenicity islands LEE, OI-122, and OI-57, the acid fitness island, and the tellurite resistance island were detected between the O145:H28 and reference strains. A great amount of genetic variation was detected in O145:H28, which was mainly attributed to deletions, insertions, and gene acquisition at several chromosomal “hot spots”. Finally, our study demonstrated a distinct virulence gene repertoire among the STEC O145:H28 strains originating from the same geographical region and revealed unforeseen contributions of loss-of-function mutations to virulence evolution and genetic diversification in STEC.},
doi = {10.3390/microorganisms10050866},
journal = {Microorganisms},
number = 5,
volume = 10,
place = {United States},
year = {Thu Apr 21 00:00:00 EDT 2022},
month = {Thu Apr 21 00:00:00 EDT 2022}
}

Works referenced in this record:

Comparative Genomics of Recent Shiga Toxin-Producing Escherichia coli O104:H4: Short-Term Evolution of an Emerging Pathogen
journal, March 2013

  • Grad, Yonatan H.; Godfrey, Paul; Cerquiera, Gustavo C.
  • mBio, Vol. 4, Issue 1
  • DOI: 10.1128/mBio.00452-12

The complete DNA sequence and analysis of the large virulence plasmid of Escherichia coli O157:H7
journal, September 1998


Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity
journal, November 2004


Origins of the E. coli Strain Causing an Outbreak of Hemolytic–Uremic Syndrome in Germany
journal, August 2011

  • Rasko, David A.; Webster, Dale R.; Sahl, Jason W.
  • New England Journal of Medicine, Vol. 365, Issue 8
  • DOI: 10.1056/NEJMoa1106920

Roary: rapid large-scale prokaryote pan genome analysis
journal, July 2015


The Type VI Secretion System in Escherichia coli and Related Species
journal, January 2016


Enteropathogenic E. coli translocated intimin receptor, Tir, interacts directly with α-actinin
journal, June 2000


EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157:H7 that contributes to adhesion and biofilm formation
journal, March 2008


Bacterial Adaptation through Loss of Function
journal, July 2013


Differential induction of Shiga toxin in environmental Escherichia coli O145:H28 strains carrying the same genotype as the outbreak strains
journal, February 2021


Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths
journal, January 2009


TheEscherichia coliO157:H7 EhaB autotransporter protein binds to laminin and collagen I and induces a serum IgA response in O157:H7 challenged cattle
journal, July 2009


Adaptive Evolution of Class 5 Fimbrial Genes in Enterotoxigenic Escherichia coli and Its Functional Consequences
journal, February 2012

  • Chattopadhyay, Sujay; Tchesnokova, Veronika; McVeigh, Annette
  • Journal of Biological Chemistry, Vol. 287, Issue 9
  • DOI: 10.1074/jbc.M111.303735

Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli
journal, October 2009

  • Ogura, Y.; Ooka, T.; Iguchi, A.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 42
  • DOI: 10.1073/pnas.0903585106

The Accessory Genome of Shiga Toxin-Producing Escherichia coli Defines a Persistent Colonization Type in Cattle
journal, September 2016

  • Barth, Stefanie A.; Menge, Christian; Eichhorn, Inga
  • Applied and Environmental Microbiology, Vol. 82, Issue 17
  • DOI: 10.1128/AEM.00909-16

The Ecology and Evolution of Pangenomes
journal, October 2019

  • Brockhurst, Michael A.; Harrison, Ellie; Hall, James P. J.
  • Current Biology, Vol. 29, Issue 20
  • DOI: 10.1016/j.cub.2019.08.012

An Environmental Shiga Toxin-Producing Escherichia coli O145 Clonal Population Exhibits High-Level Phenotypic Variation That Includes Virulence Traits
journal, February 2016

  • Carter, Michelle Qiu; Quinones, Beatriz; He, Xiaohua
  • Applied and Environmental Microbiology, Vol. 82, Issue 4
  • DOI: 10.1128/AEM.03172-15

Functional Analysis of Genes Comprising the Locus of Heat Resistance in Escherichia coli
journal, October 2017

  • Mercer, Ryan; Nguyen, Oanh; Ou, Qixing
  • Applied and Environmental Microbiology, Vol. 83, Issue 20
  • DOI: 10.1128/AEM.01400-17

Aspects of genome plasticity in pathogenic Escherichia coli
journal, November 2007

  • Bielaszewska, Martina; Dobrindt, Ulrich; Gärtner, Julia
  • International Journal of Medical Microbiology, Vol. 297, Issue 7-8
  • DOI: 10.1016/j.ijmm.2007.03.001

CfaE tip mutations in enterotoxigenicEscherichia coliCFA/I fimbriae define critical human intestinal binding sites
journal, May 2009


Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study
journal, September 2011


Locus of Adhesion and Autoaggregation (LAA), a pathogenicity island present in emerging Shiga Toxin–producing Escherichia coli strains
journal, August 2017


VFDB 2022: a general classification scheme for bacterial virulence factors
journal, November 2021

  • Liu, Bo; Zheng, Dandan; Zhou, Siyu
  • Nucleic Acids Research, Vol. 50, Issue D1
  • DOI: 10.1093/nar/gkab1107

Genetic determinants of heat resistance in Escherichia coli
journal, September 2015

  • Mercer, Ryan G.; Zheng, Jinshui; Garcia-Hernandez, Rigoberto
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00932

The Complete Genome Sequence of Escherichia coli K-12
journal, September 1997


Role of outer membrane barrier in efflux-mediated tetracycline resistance of Escherichia coli.
journal, February 1995


Non‐O157 Shiga Toxin–Producing Escherichia coli Infections in the United States, 1983–2002
journal, October 2005

  • Brooks, John T.; Sowers, Evangeline G.; Wells, Joy G.
  • The Journal of Infectious Diseases, Vol. 192, Issue 8
  • DOI: 10.1086/466536

The evolution of the Escherichia coli phylogeny
journal, March 2012


Differential dynamics and impacts of prophages and plasmids on the pangenome and virulence factor repertoires of Shiga toxin-producing Escherichia coli O145:H28
journal, January 2020

  • Nakamura, Keiji; Murase, Kazunori; Sato, Mitsuhiko P.
  • Microbial Genomics, Vol. 6, Issue 1
  • DOI: 10.1099/mgen.0.000323

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

Conditional Function of Autoaggregative Protein Cah and Common cah Mutations in Shiga Toxin-Producing Escherichia coli
journal, January 2018

  • Carter, Michelle Qiu; Brandl, Maria T.; Kudva, Indira T.
  • Applied and Environmental Microbiology, Vol. 84, Issue 1
  • DOI: 10.1128/AEM.01739-17

A new pathogenicity island carrying an allelic variant of the Subtilase cytotoxin is common among Shiga toxin producing Escherichia coli of human and ovine origin
journal, March 2013

  • Michelacci, V.; Tozzoli, R.; Caprioli, A.
  • Clinical Microbiology and Infection, Vol. 19, Issue 3
  • DOI: 10.1111/1469-0691.12122

IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets
journal, May 2017

  • Bertelli, Claire; Laird, Matthew R.; Williams, Kelly P.
  • Nucleic Acids Research, Vol. 45, Issue W1
  • DOI: 10.1093/nar/gkx343

CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2
journal, August 2005


ModelFinder: fast model selection for accurate phylogenetic estimates
journal, May 2017

  • Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F.
  • Nature Methods, Vol. 14, Issue 6
  • DOI: 10.1038/nmeth.4285

High-Quality Whole-Genome Sequences for 77 Shiga Toxin-Producing Escherichia coli Strains Generated with PacBio Sequencing
journal, May 2018

  • Patel, Pooja N.; Lindsey, Rebecca L.; Garcia-Toledo, Lisley
  • Genome Announcements, Vol. 6, Issue 19
  • DOI: 10.1128/genomeA.00391-18

VFDB 2019: a comparative pathogenomic platform with an interactive web interface
journal, November 2018

  • Liu, Bo; Zheng, Dandan; Jin, Qi
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1080

Genes under positive selection in Escherichia coli
journal, July 2007

  • Petersen, L.; Bollback, J. P.; Dimmic, M.
  • Genome Research, Vol. 17, Issue 9
  • DOI: 10.1101/gr.6254707

Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes
journal, May 2015

  • Denamur, Erick; Clermont, Olivier; Gordon, David
  • Microbiology, Vol. 161, Issue 5
  • DOI: 10.1099/mic.0.000063

OI-57, a Genomic Island of Escherichia coli O157, Is Present in Other Seropathotypes of Shiga Toxin-Producing E. coli Associated with Severe Human Disease
journal, November 2010

  • Imamovic, Lejla; Tozzoli, Rosangela; Michelacci, Valeria
  • Infection and Immunity, Vol. 78, Issue 11
  • DOI: 10.1128/IAI.00512-10

Insights from 20 years of bacterial genome sequencing
journal, February 2015

  • Land, Miriam; Hauser, Loren; Jun, Se-Ran
  • Functional & Integrative Genomics, Vol. 15, Issue 2
  • DOI: 10.1007/s10142-015-0433-4

Outbreaks of non-O157 Shiga toxin-producing Escherichia coli infection: USA
journal, January 2014

  • Luna-Gierke, R. E.; Griffin, P. M.; Gould, L. H.
  • Epidemiology and Infection, Vol. 142, Issue 11
  • DOI: 10.1017/S0950268813003233

IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era
journal, February 2020

  • Minh, Bui Quang; Schmidt, Heiko A.; Chernomor, Olga
  • Molecular Biology and Evolution, Vol. 37, Issue 5
  • DOI: 10.1093/molbev/msaa015

Support vector machine applied to predict the zoonotic potential of E. coli O157 cattle isolates
journal, September 2016

  • Lupolova, Nadejda; Dallman, Timothy J.; Matthews, Louise
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 40
  • DOI: 10.1073/pnas.1606567113

Differential Stability and Trade-Off Effects of Pathoadaptive Mutations in the Escherichia coli FimH Adhesin
journal, July 2007

  • Weissman, Scott J.; Beskhlebnaya, Viktoriya; Chesnokova, Veronika
  • Infection and Immunity, Vol. 75, Issue 7
  • DOI: 10.1128/IAI.01963-06

Prevalence of the “High-Pathogenicity Island” of Yersinia Species among Escherichia coli Strains That Are Pathogenic to Humans
journal, February 1998


Natural rpoS mutations contribute to population heterogeneity in Escherichia coli O157:H7 strains linked to the 2006 US spinach-associated outbreak
journal, December 2014


Genome sequence of enterohaemorrhagic Escherichia coli O157:H7
journal, January 2001

  • Perna, Nicole T.; Plunkett, Guy; Burland, Valerie
  • Nature, Vol. 409, Issue 6819
  • DOI: 10.1038/35054089

Rapid and Easy In Silico Serotyping of Escherichia coli Isolates by Use of Whole-Genome Sequencing Data
journal, May 2015

  • Joensen, Katrine G.; Tetzschner, Anna M. M.; Iguchi, Atsushi
  • Journal of Clinical Microbiology, Vol. 53, Issue 8
  • DOI: 10.1128/JCM.00008-15

Diarrheagenic Escherichia coli
journal, January 1998

  • Nataro, James P.; Kaper, James B.
  • Clinical Microbiology Reviews, Vol. 11, Issue 1
  • DOI: 10.1128/CMR.11.1.142

RcsB Contributes to the Distinct Stress Fitness among Escherichia coli O157:H7 Curli Variants of the 1993 Hamburger-Associated Outbreak Strains
journal, November 2012

  • Carter, Michelle Q.; Parker, Craig T.; Louie, Jacqueline W.
  • Applied and Environmental Microbiology, Vol. 78, Issue 21
  • DOI: 10.1128/AEM.02157-12

The Evolution of Virulence in Non-O157 Shiga Toxin-Producing Escherichia Coli
journal, January 2011

  • Coombes, Brian K.; Gilmour, Matthew W.; Goodman, Chelsey D.
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00090

Products of the Escherichia coli Acid Fitness Island Attenuate Metabolite Stress at Extremely Low pH and Mediate a Cell Density-Dependent Acid Resistance
journal, April 2007

  • Mates, Aaron K.; Sayed, Atef K.; Foster, John W.
  • Journal of Bacteriology, Vol. 189, Issue 7
  • DOI: 10.1128/JB.01490-06

The Functions of Effector Proteins in Yersinia Virulence
journal, January 2016


The Pangenome Structure of Escherichia coli: Comparative Genomic Analysis of E. coli Commensal and Pathogenic Isolates
journal, August 2008

  • Rasko, David A.; Rosovitz, M. J.; Myers, Garry S. A.
  • Journal of Bacteriology, Vol. 190, Issue 20
  • DOI: 10.1128/JB.00619-08

Uropathogenic Escherichia coli Modulates Immune Responses and Its Curli Fimbriae Interact with the Antimicrobial Peptide LL-37
journal, July 2010


Species-Wide Variation in the Escherichia coli Flagellin (H-Antigen) Gene
journal, May 2003


Why prokaryotes have pangenomes
journal, March 2017


Decoding the Ecological Function of Accessory Genome
journal, January 2017


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

A complete view of the genetic diversity of the Escherichia coli O-antigen biosynthesis gene cluster
journal, November 2014


Expression of and Cytokine Activation byEscherichia coliCurli Fibers in Human Sepsis
journal, February 2000

  • Bian, Zhao; Brauner, Annelie; Li, Yinghua
  • The Journal of Infectious Diseases, Vol. 181, Issue 2
  • DOI: 10.1086/315233

Cumulative acquisition of pathogenicity islands has shaped virulence potential and contributed to the emergence of LEE-negative Shiga toxin-producing Escherichia coli strains
journal, January 2019


Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis
journal, July 2011

  • Rohmer, Laurence; Hocquet, Didier; Miller, Samuel I.
  • Trends in Microbiology, Vol. 19, Issue 7
  • DOI: 10.1016/j.tim.2011.04.003

Chromosomal instability in enterohaemorrhagic Escherichia coli O157:H7: impact on adherence, tellurite resistance and colony phenotype
journal, January 2011


Genomic islands: tools of bacterial horizontal gene transfer and evolution
journal, March 2009