Genomic analysis of factors associated with low prevalence of antibiotic resistance in extraintestinal pathogenic Escherichia coli sequence type 95 strains

Craig M. Stephens; Sheila Adams-Sapper; Manraj Sekhon; James R. Johnson; Lee W. Riley

doi:10.1128/mSphere.00390-16

Genomic analysis of factors associated with low prevalence of antibiotic resistance in extraintestinal pathogenic Escherichia coli sequence type 95 strains

Craig M. Stephens, Sheila Adams-Sapper, Manraj Sekhon, James R. Johnson, Lee W. Riley

Medicine - Veteran's Administration Medical Center

Research output: Contribution to journal › Article › peer-review

38 Scopus citations

Abstract

Extraintestinal pathogenic Escherichia coli (ExPEC) strains belonging to multilocus sequence type 95 (ST95) are globally distributed and a common cause of infections in humans and domestic fowl. ST95 isolates generally show a lower prevalence of acquired antimicrobial resistance than other pandemic ExPEC lineages. We took a genomic approach to identify factors that may underlie reduced resistance. We fully assembled genomes for four ST95 isolates representing the four major fimH-based lineages within ST95 and also analyzed draft-level genomes from another 82 ST95 isolates, largely from the western United States. The fully assembled genomes of antibiotic-resistant isolates carried resistance genes exclusively on large (> 90-kb) IncFIB/IncFII plasmids. These replicons were common in the draft genomes as well, particularly in antibiotic-resistant isolates, but we also observed multiple instances of a smaller (8.3-kb) ampicillin resistance plasmid that had been previously identified in Salmonella enterica. Among ST95 isolates, pansusceptibility to antibiotics was significantly associated with the fimH6 lineage and the presence of homologs of the previously identified 114-kb IncFIB/IncFII plasmid pUTI89, both of which were also associated with reduced carriage of other plasmids. Potential mechanistic explanations for lineage- and plasmid-specific effects on the prevalence of antibiotic resistance within the ST95 group are discussed.

Original language	English (US)
Article number	e00390-16
Journal	mSphere
Volume	2
Issue number	2
DOIs	https://doi.org/10.1128/mSphere.00390-16
State	Published - Mar 1 2017

Bibliographical note

Funding Information:
We thank Brian Johnston in the Johnson lab for sharing ST95 isolates. We thank Jeffrey Skerker for assistance with analysis of methylation sites from SMRT sequencing data and Nicole Tarlton for thoughtful comments on the manuscript. Finally, we thank Taylor Kelly, Charles Lee, Christopher Alvarado, Jack McBride, and Eric Jedel for contributions to bioinformatics analysis of the ST95 isolates. This work used the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 Instrumentation grants S10RR029668 and S10RR027303. The work was supported by the R. B. Roberts Fund provided to the Riley lab. This material is also based in part on work supported by Office of Research and Development, Medical Research Service, Department of Veterans Affairs, grant 1 I01 CX000920-01 (J.R.J.)

Publisher Copyright:
© 2017 Stephens et al.

Keywords

Antibiotic resistance
Escherichia coli
ExPEC
Genomics
ST95

Publisher link

10.1128/mSphere.00390-16

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5381267

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title = "Genomic analysis of factors associated with low prevalence of antibiotic resistance in extraintestinal pathogenic Escherichia coli sequence type 95 strains",

abstract = "Extraintestinal pathogenic Escherichia coli (ExPEC) strains belonging to multilocus sequence type 95 (ST95) are globally distributed and a common cause of infections in humans and domestic fowl. ST95 isolates generally show a lower prevalence of acquired antimicrobial resistance than other pandemic ExPEC lineages. We took a genomic approach to identify factors that may underlie reduced resistance. We fully assembled genomes for four ST95 isolates representing the four major fimH-based lineages within ST95 and also analyzed draft-level genomes from another 82 ST95 isolates, largely from the western United States. The fully assembled genomes of antibiotic-resistant isolates carried resistance genes exclusively on large (> 90-kb) IncFIB/IncFII plasmids. These replicons were common in the draft genomes as well, particularly in antibiotic-resistant isolates, but we also observed multiple instances of a smaller (8.3-kb) ampicillin resistance plasmid that had been previously identified in Salmonella enterica. Among ST95 isolates, pansusceptibility to antibiotics was significantly associated with the fimH6 lineage and the presence of homologs of the previously identified 114-kb IncFIB/IncFII plasmid pUTI89, both of which were also associated with reduced carriage of other plasmids. Potential mechanistic explanations for lineage- and plasmid-specific effects on the prevalence of antibiotic resistance within the ST95 group are discussed.",

keywords = "Antibiotic resistance, Escherichia coli, ExPEC, Genomics, ST95",

author = "Stephens, {Craig M.} and Sheila Adams-Sapper and Manraj Sekhon and Johnson, {James R.} and Riley, {Lee W.}",

note = "Funding Information: We thank Brian Johnston in the Johnson lab for sharing ST95 isolates. We thank Jeffrey Skerker for assistance with analysis of methylation sites from SMRT sequencing data and Nicole Tarlton for thoughtful comments on the manuscript. Finally, we thank Taylor Kelly, Charles Lee, Christopher Alvarado, Jack McBride, and Eric Jedel for contributions to bioinformatics analysis of the ST95 isolates. This work used the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 Instrumentation grants S10RR029668 and S10RR027303. The work was supported by the R. B. Roberts Fund provided to the Riley lab. This material is also based in part on work supported by Office of Research and Development, Medical Research Service, Department of Veterans Affairs, grant 1 I01 CX000920-01 (J.R.J.) Publisher Copyright: {\textcopyright} 2017 Stephens et al.",

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doi = "10.1128/mSphere.00390-16",

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AU - Riley, Lee W.

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N2 - Extraintestinal pathogenic Escherichia coli (ExPEC) strains belonging to multilocus sequence type 95 (ST95) are globally distributed and a common cause of infections in humans and domestic fowl. ST95 isolates generally show a lower prevalence of acquired antimicrobial resistance than other pandemic ExPEC lineages. We took a genomic approach to identify factors that may underlie reduced resistance. We fully assembled genomes for four ST95 isolates representing the four major fimH-based lineages within ST95 and also analyzed draft-level genomes from another 82 ST95 isolates, largely from the western United States. The fully assembled genomes of antibiotic-resistant isolates carried resistance genes exclusively on large (> 90-kb) IncFIB/IncFII plasmids. These replicons were common in the draft genomes as well, particularly in antibiotic-resistant isolates, but we also observed multiple instances of a smaller (8.3-kb) ampicillin resistance plasmid that had been previously identified in Salmonella enterica. Among ST95 isolates, pansusceptibility to antibiotics was significantly associated with the fimH6 lineage and the presence of homologs of the previously identified 114-kb IncFIB/IncFII plasmid pUTI89, both of which were also associated with reduced carriage of other plasmids. Potential mechanistic explanations for lineage- and plasmid-specific effects on the prevalence of antibiotic resistance within the ST95 group are discussed.

AB - Extraintestinal pathogenic Escherichia coli (ExPEC) strains belonging to multilocus sequence type 95 (ST95) are globally distributed and a common cause of infections in humans and domestic fowl. ST95 isolates generally show a lower prevalence of acquired antimicrobial resistance than other pandemic ExPEC lineages. We took a genomic approach to identify factors that may underlie reduced resistance. We fully assembled genomes for four ST95 isolates representing the four major fimH-based lineages within ST95 and also analyzed draft-level genomes from another 82 ST95 isolates, largely from the western United States. The fully assembled genomes of antibiotic-resistant isolates carried resistance genes exclusively on large (> 90-kb) IncFIB/IncFII plasmids. These replicons were common in the draft genomes as well, particularly in antibiotic-resistant isolates, but we also observed multiple instances of a smaller (8.3-kb) ampicillin resistance plasmid that had been previously identified in Salmonella enterica. Among ST95 isolates, pansusceptibility to antibiotics was significantly associated with the fimH6 lineage and the presence of homologs of the previously identified 114-kb IncFIB/IncFII plasmid pUTI89, both of which were also associated with reduced carriage of other plasmids. Potential mechanistic explanations for lineage- and plasmid-specific effects on the prevalence of antibiotic resistance within the ST95 group are discussed.

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KW - Genomics

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ER -

Genomic analysis of factors associated with low prevalence of antibiotic resistance in extraintestinal pathogenic Escherichia coli sequence type 95 strains

Abstract

Bibliographical note

Keywords

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