The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coli

ABSTRACT Escherichia coli strains of phylogenetic group B2 are often associated with urinary tract infections (UTIs) and several other diseases. Recent genomic and transcriptomic analyses have not suggested or identified specific genes required for virulence, but have instead suggested multiple viru...

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Main Authors: Jacob Hogins, Zhenyu Xuan, Philippe E. Zimmern, Larry Reitzer
Format: Article
Language:English
Published: American Society for Microbiology 2023-10-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02085-23
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author Jacob Hogins
Zhenyu Xuan
Philippe E. Zimmern
Larry Reitzer
author_facet Jacob Hogins
Zhenyu Xuan
Philippe E. Zimmern
Larry Reitzer
author_sort Jacob Hogins
collection DOAJ
description ABSTRACT Escherichia coli strains of phylogenetic group B2 are often associated with urinary tract infections (UTIs) and several other diseases. Recent genomic and transcriptomic analyses have not suggested or identified specific genes required for virulence, but have instead suggested multiple virulence strategies and complex host-pathogen interactions. Previous analyses have not compared core gene expression between phylogenetic groups or between pathogens and nonpathogens within phylogenetic groups. We compared the core gene expression of 35 strains from three phylogenetic groups that included both pathogens and nonpathogens after growth in a medium that allowed comparable growth of both types of strains. K-means clustering suggested a B2 cluster with 17 group B2 strains and two group A strains; an AD cluster with six group A strains, five group D strains and one B2 strain; and four outliers which included the highly studied model uropathogenic E. coli strains UTI89 and CFT073. Half of the core genes were differentially expressed between B2 and AD cluster strains, including transcripts of genes for all aspects of macromolecular synthesis—replication, transcription, translation, and peptidoglycan synthesis—energy metabolism, and environmental-sensing transcriptional regulators. Notably, core gene expression between nonpathogenic and uropathogenic transcriptomes within phylogenetic groups did not differ. If differences between pathogens and nonpathogens exist, then the differences do not require transcriptional reprogramming. In summary, B2 cluster strains have a distinct transcription pattern that involves hundreds of genes. We propose that this transcription pattern is one factor that contributes to virulence. IMPORTANCE Escherichia coli is a diverse species and an opportunistic pathogen that is associated with various diseases, such as urinary tract infections. When examined, phylogenetic group B2 strains are more often associated with these diseases, but the specific properties that contribute to their virulence are not known. From a comparative transcriptomic analysis, we found that group B2 strains grown in a nutrient-rich medium had a distinct transcription pattern, which is the first evidence that core gene expression differs between phylogenetic groups. Understanding the consequences of group B2 transcription pattern will provide important information on basic E. coli biology, the basis for E. coli virulence, and possibly for developing therapies for a majority of urinary tract infections and other group B2-associated diseases.
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spelling doaj.art-39a23425eac44f2caebeddab021ec7b02023-10-17T13:04:35ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-10-0111510.1128/spectrum.02085-23The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coliJacob Hogins0Zhenyu Xuan1Philippe E. Zimmern2Larry Reitzer3Department of Biological Sciences, The University of Texas at Dallas , Richardson, Texas, USADepartment of Biological Sciences, The University of Texas at Dallas , Richardson, Texas, USADepartment of Urology, The University of Texas Southwestern , Dallas, Texas, USADepartment of Biological Sciences, The University of Texas at Dallas , Richardson, Texas, USAABSTRACT Escherichia coli strains of phylogenetic group B2 are often associated with urinary tract infections (UTIs) and several other diseases. Recent genomic and transcriptomic analyses have not suggested or identified specific genes required for virulence, but have instead suggested multiple virulence strategies and complex host-pathogen interactions. Previous analyses have not compared core gene expression between phylogenetic groups or between pathogens and nonpathogens within phylogenetic groups. We compared the core gene expression of 35 strains from three phylogenetic groups that included both pathogens and nonpathogens after growth in a medium that allowed comparable growth of both types of strains. K-means clustering suggested a B2 cluster with 17 group B2 strains and two group A strains; an AD cluster with six group A strains, five group D strains and one B2 strain; and four outliers which included the highly studied model uropathogenic E. coli strains UTI89 and CFT073. Half of the core genes were differentially expressed between B2 and AD cluster strains, including transcripts of genes for all aspects of macromolecular synthesis—replication, transcription, translation, and peptidoglycan synthesis—energy metabolism, and environmental-sensing transcriptional regulators. Notably, core gene expression between nonpathogenic and uropathogenic transcriptomes within phylogenetic groups did not differ. If differences between pathogens and nonpathogens exist, then the differences do not require transcriptional reprogramming. In summary, B2 cluster strains have a distinct transcription pattern that involves hundreds of genes. We propose that this transcription pattern is one factor that contributes to virulence. IMPORTANCE Escherichia coli is a diverse species and an opportunistic pathogen that is associated with various diseases, such as urinary tract infections. When examined, phylogenetic group B2 strains are more often associated with these diseases, but the specific properties that contribute to their virulence are not known. From a comparative transcriptomic analysis, we found that group B2 strains grown in a nutrient-rich medium had a distinct transcription pattern, which is the first evidence that core gene expression differs between phylogenetic groups. Understanding the consequences of group B2 transcription pattern will provide important information on basic E. coli biology, the basis for E. coli virulence, and possibly for developing therapies for a majority of urinary tract infections and other group B2-associated diseases.https://journals.asm.org/doi/10.1128/spectrum.02085-23Escherichia colipathogensurinary tract infectiontranscriptional regulationtranscription factorsphylogenetic analysis
spellingShingle Jacob Hogins
Zhenyu Xuan
Philippe E. Zimmern
Larry Reitzer
The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coli
Microbiology Spectrum
Escherichia coli
pathogens
urinary tract infection
transcriptional regulation
transcription factors
phylogenetic analysis
title The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coli
title_full The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coli
title_fullStr The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coli
title_full_unstemmed The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coli
title_short The distinct transcriptome of virulence-associated phylogenetic group B2 Escherichia coli
title_sort distinct transcriptome of virulence associated phylogenetic group b2 escherichia coli
topic Escherichia coli
pathogens
urinary tract infection
transcriptional regulation
transcription factors
phylogenetic analysis
url https://journals.asm.org/doi/10.1128/spectrum.02085-23
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