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Journal of Bacteriology, June 2009, p. 3553-3568, Vol. 191, No. 11
0021-9193/09/$08.00+0     doi:10.1128/JB.01738-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

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{triangledown}

Zhijie Yang,1 Jaehyoung Kim,1 Chaomei Zhang,1 Min Zhang,1 Joeseph Nietfeldt,1 Carolyn M. Southward,2 Michael G. Surette,2,3 Stephen D. Kachman,4 and Andrew K. Benson1*

Department of Food Science and Technology,1 Department of Statistics, University of Nebraska, Lincoln, Nebraska 68583-0919,4 Department of Microbiology and Infectious Diseases,2 Department of Biochemistry and Molecular Biology, Health Sciences Center, University of Calgary, Alberta, Canada T2N4N13

Received 11 December 2008/ Accepted 19 March 2009

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.

* Corresponding author. Mailing address: Department of Food Science and Technology, University of Nebraska, 330 Food Industry Complex, Lincoln, NE 68583-0919. Phone: (402) 472-5637. Fax: (402) 472-1693. E-mail: abenson1{at}unl.edu

{triangledown} Published ahead of print on 27 March 2009.

Journal of Bacteriology, June 2009, p. 3553-3568, Vol. 191, No. 11
0021-9193/09/$08.00+0     doi:10.1128/JB.01738-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



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