Genomic instability in regions adjacent to a highly conserved pch prophage in Escherichia coli O157:H7 generates diversity in expression patterns of the LEE pathogenicity island

Zhijie Yang, Jaehyoung Kim, Chaomei Zhang, Min Zhang, Joeseph Nietfeldt, Carolyn M. Southward, Michael G. Surette, Stephen D. Kachman, Andrew K. Benson

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

The LEE pathogenicity island has been acquired on multiple occasions within the different lineages of enteropathogenic and enterohemorrhagic Escherichia coli. In each lineage, LEE expression is regulated by complex networks of pathways, including core pathways shared by all lineages and lineage-specific pathways. Within the O157:H7 lineage of enterohemorrhagic E. coli, strain-to-strain variation in LEE expression has been observed, implying that expression patterns can diversify even within highly related subpopulations. Using comparative genomics of E. coli O157:H7 subpopulations, we have identified one source of strain-level variation affecting LEE expression. The variation occurs in prophage-dense regions of the genome that lie immediately adjacent to the late regions of the pch prophage carrying pchA, pchB, pchC, and a newly identified pch gene, pchX. Genomic segments extending from the holin S region to the pchA, pchB, pchC, and pchX genes of their respective prophage are highly conserved but are nonetheless embedded within adjacent genomic segments that are extraordinarily variable, termed pch adjacent genomic regions (pch AGR). Despite the remarkable degree of variation, the pattern of variation in pch AGR is highly correlated with the distribution of phylogenetic markers on the backbone of the genome. Quantitative analysis of transcription from the LEE1 promoter further revealed that variation in the pch AGR has substantial effects on absolute levels and patterns of LEE1 transcription. Variation in the pch AGR therefore serves as a mechanism to diversify LEE expression patterns, and the lineage-specific pattern of pch AGR variation could ultimately influence ecological or virulence characteristics of subpopulations within each lineage.

Original languageEnglish (US)
Pages (from-to)3553-3568
Number of pages16
JournalJournal of bacteriology
Volume191
Issue number11
DOIs
StatePublished - Jun 1 2009

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Prophages
Genomic Islands
Escherichia coli O157
Genomic Instability
Enterohemorrhagic Escherichia coli
Genome
Enteropathogenic Escherichia coli
Genomics
Genes
Virulence

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Genomic instability in regions adjacent to a highly conserved pch prophage in Escherichia coli O157:H7 generates diversity in expression patterns of the LEE pathogenicity island. / Yang, Zhijie; Kim, Jaehyoung; Zhang, Chaomei; Zhang, Min; Nietfeldt, Joeseph; Southward, Carolyn M.; Surette, Michael G.; Kachman, Stephen D.; Benson, Andrew K.

In: Journal of bacteriology, Vol. 191, No. 11, 01.06.2009, p. 3553-3568.

Research output: Contribution to journalArticle

Yang, Zhijie ; Kim, Jaehyoung ; Zhang, Chaomei ; Zhang, Min ; Nietfeldt, Joeseph ; Southward, Carolyn M. ; Surette, Michael G. ; Kachman, Stephen D. ; Benson, Andrew K. / Genomic instability in regions adjacent to a highly conserved pch prophage in Escherichia coli O157:H7 generates diversity in expression patterns of the LEE pathogenicity island. In: Journal of bacteriology. 2009 ; Vol. 191, No. 11. pp. 3553-3568.
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abstract = "The LEE pathogenicity island has been acquired on multiple occasions within the different lineages of enteropathogenic and enterohemorrhagic Escherichia coli. In each lineage, LEE expression is regulated by complex networks of pathways, including core pathways shared by all lineages and lineage-specific pathways. Within the O157:H7 lineage of enterohemorrhagic E. coli, strain-to-strain variation in LEE expression has been observed, implying that expression patterns can diversify even within highly related subpopulations. Using comparative genomics of E. coli O157:H7 subpopulations, we have identified one source of strain-level variation affecting LEE expression. The variation occurs in prophage-dense regions of the genome that lie immediately adjacent to the late regions of the pch prophage carrying pchA, pchB, pchC, and a newly identified pch gene, pchX. Genomic segments extending from the holin S region to the pchA, pchB, pchC, and pchX genes of their respective prophage are highly conserved but are nonetheless embedded within adjacent genomic segments that are extraordinarily variable, termed pch adjacent genomic regions (pch AGR). Despite the remarkable degree of variation, the pattern of variation in pch AGR is highly correlated with the distribution of phylogenetic markers on the backbone of the genome. Quantitative analysis of transcription from the LEE1 promoter further revealed that variation in the pch AGR has substantial effects on absolute levels and patterns of LEE1 transcription. Variation in the pch AGR therefore serves as a mechanism to diversify LEE expression patterns, and the lineage-specific pattern of pch AGR variation could ultimately influence ecological or virulence characteristics of subpopulations within each lineage.",
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AU - Kim, Jaehyoung

AU - Zhang, Chaomei

AU - Zhang, Min

AU - Nietfeldt, Joeseph

AU - Southward, Carolyn M.

AU - Surette, Michael G.

AU - Kachman, Stephen D.

AU - Benson, Andrew K.

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AB - The LEE pathogenicity island has been acquired on multiple occasions within the different lineages of enteropathogenic and enterohemorrhagic Escherichia coli. In each lineage, LEE expression is regulated by complex networks of pathways, including core pathways shared by all lineages and lineage-specific pathways. Within the O157:H7 lineage of enterohemorrhagic E. coli, strain-to-strain variation in LEE expression has been observed, implying that expression patterns can diversify even within highly related subpopulations. Using comparative genomics of E. coli O157:H7 subpopulations, we have identified one source of strain-level variation affecting LEE expression. The variation occurs in prophage-dense regions of the genome that lie immediately adjacent to the late regions of the pch prophage carrying pchA, pchB, pchC, and a newly identified pch gene, pchX. Genomic segments extending from the holin S region to the pchA, pchB, pchC, and pchX genes of their respective prophage are highly conserved but are nonetheless embedded within adjacent genomic segments that are extraordinarily variable, termed pch adjacent genomic regions (pch AGR). Despite the remarkable degree of variation, the pattern of variation in pch AGR is highly correlated with the distribution of phylogenetic markers on the backbone of the genome. Quantitative analysis of transcription from the LEE1 promoter further revealed that variation in the pch AGR has substantial effects on absolute levels and patterns of LEE1 transcription. Variation in the pch AGR therefore serves as a mechanism to diversify LEE expression patterns, and the lineage-specific pattern of pch AGR variation could ultimately influence ecological or virulence characteristics of subpopulations within each lineage.

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