Source: IOWA STATE UNIVERSITY submitted to
POSSIBLE EMERGENCE OF PLASMID-CONTAINING APEC STRAINS IN POULTRY
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
0205935
Grant No.
(N/A)
Project No.
IOWV-JOHN-411-23-30
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Dec 1, 2005
Project End Date
Nov 30, 2006
Grant Year
(N/A)
Project Director
JOHNSON, T. J.
Recipient Organization
IOWA STATE UNIVERSITY
S. AND 16TH ELWOOD
AMES,IA 50011
Performing Department
VETERINARY MEDICINE
Non Technical Summary
Despite the economic importance of avian colibacillosis, the mechanisms of virulence employed by avian pathogenic Escherichia coli (APEC) have long remained a puzzle, confounding efforts to control the disease. However, in recent years, a widespread attribute of these organisms has been recognized that provides a focus for their study. It is the presence of large plasmids. We propose the sequencing of a large APEC resistance plasmid, and subsequent use of the data generated to produce an E. coli plasmid microarray that will be used to scan APEC isolated over the past 35 years for plasmid-associated sequences. The results obtained in the proposed project will allow us to determine if plasmid-containing strains of APEC have emerged in the poultry environment. It will also offer us an opportunity to explore the evolution of plasmid-mediated virulence and antimicrobial resistance among E. coli.
Animal Health Component
100%
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
31132991040100%
Knowledge Area
311 - Animal Diseases;

Subject Of Investigation
3299 - Poultry, general/other;

Field Of Science
1040 - Molecular biology;
Goals / Objectives
Despite the economic importance of avian colibacillosis, the mechanisms of virulence employed by avian pathogenic Escherichia coli (APEC) have long remained a puzzle, confounding efforts to control the disease. However, in recent years, a widespread attribute of these organisms has been recognized that provides a focus for their study. It is the presence of large plasmids. These plasmids encode antimicrobial resistance and virulence, and they are significantly more likely to be found in APEC than in commensal E. coli of healthy birds. Interestingly, plasmid-associated virulence factors, and the large plasmids that encode them, appear to have recently emerged as a defining feature of APEC. In the present study, we propose testing the hypothesis that plasmid-containing APEC have recently emerged via comparison of plasmid content and constitution among APEC isolated over the past 35 years. To do this, we will use a comprehensive E. coli "plasmid chip", created with DNA microarray technology. To support this study, we have generated the first APEC plasmid sequences, including two large virulence plasmids (the first ColV and ColBM plasmids sequenced), as well as two large R plasmids. Here, we propose the sequencing of an additional large APEC IncN plasmid, as it is representative of a type of plasmid that occurs commonly in present day APEC isolates and it is the only APEC plasmid type yet to be sequenced. We can then use comparative genomics to discern similarities and differences among APEC plasmids. The sequence data obtained will also be used to produce an E. coli plasmid chip that will be used to scan APEC, isolated over the past 35 years, for plasmid-associated sequences. From these results, we will be able to determine if plasmid-containing strains of APEC have emerged in the poultry environment. It will also offer us an opportunity to explore the evolution of plasmid-mediated virulence and antimicrobial resistance among E. coli.
Project Methods
SPECIFIC OBJECTIVE 1. Completely sequence a 100-kb IncN plasmid from an APEC strain. Methods. Shotgun sequencing, assembly, and finishing will be performed on the 100-kb IncN APEC plasmid. Plasmid DNA will be prepared according to the methods of Wang and Rossman, sheared, concentrated and desalted using standard protocols. One thousand clones will be picked and arrayed in an effort to obtain eight-fold sequencing coverage. Bi-directional shotgun sequencing will be performed by MWG Biotech, Inc. The data will be collected with ABI 3700 and ABI 3730xl capillary sequencers and assembled using the SeqMan program from DNASTAR. Assembly and finishing will be perfomed by the PI, Tim Johnson, and will involve an optimized multiplex PCR procedure. Any remaining gaps in the plasmid sequences will be resolved using high-stringency PCR. SPECIFIC OBJECTIVE 2. Analyze and compare the sequences of five APEC plasmids. Methods. Open reading frames (ORFs) in the plasmid sequences will be identified using GeneQuest from DNASTAR, followed by manual inspection. Translated ORFs will then be compared to known protein sequences using the BLAST algorithm. Physical genetic maps will be created for each plasmid using Visual Cloning software. Plasmid G+C content of individual ORFs will be analyzed using GeneQuest (DNASTAR). Insertion sequences and repetitive elements will be identified using IS FINDER (http://www-is.biotoul.fr/). Genomic comparisons of the five APEC plasmid sequences obtained in our laboratory will be performed using MAUVE alignments and manual inspection. Amino acid sequence alignments will also be performed using MegAlign (DNASTAR). The codon bias of each plasmid will be analyzed using the General Codon Usage Analysis software and compared to E. coli K-12. SPECIFIC OBJECTIVE 3. Construct the comprehensive plasmid chip. Methods. Unique oligonucleotides from each of the five plasmids' genes plus others identified in the literature will be designed using Primer3 software, modified to eliminate false priming and potential cross hybridization of genome sequences. Each probe will be printed in duplicate for each array with four complete arrays printed to each glass substrate, UltraGAPS (Corning). Besides the probes being printed in non-adjacent, well-spaced duplicate locations, control spots, consisting of non-homologous DNA sequences of the same size as oligonucleotide probes, will be added. Additionally, negative control probes will be included. SPECIFIC OBJECTIVE 4. Using the chip, scan APEC isolated over the past 35 years will be scanned for plasmid genes. Methods. Total DNA will be isolated from the APEC isolates, fragmented to <800 bp by mechanical shearing and then labeled using a commercially available kit. At least 40 APEC isolates per decade (1970s, 80s, 90s, and 00s) will be used.

Progress 01/01/06 to 12/31/06

Outputs
Despite the economic importance of avian colibacillosis, the mechanisms of virulence employed by avian pathogenic Escherichia coli (APEC) have long remained a puzzle, confounding efforts to control the disease. Recent studies have identified colicin-encoding virulence plasmids as a defining trait of the APEC pathotype. Sequencing of two such plasmids identified a conserved pathogenicity island (PAI), containing a variety of virulence-associated genes, including iron acquisition and transport genes, such as those of the aerobactin, salmochelin, sit, eit, and ets systems; autotransporters/adhesins, such as tsh; hemolysins, such as hlyF; and genes involved in complement and serum resistance, such as iss and traT. APEC plasmids have been found to confer these and other beneficial properties to their host strains. In addition to virulence plasmids, possession of multidrug resistance (R) plasmids is another key characteristic of APEC. We have recently sequenced two representative APEC R plasmids and performed plasmid replicon typing and antimicrobial susceptibility testing on over 1,000 avian E. coli isolates. The results of these studies indicate a strong association between several plasmid types, class 1 integrons harboring drug resistance genes, and the ability of the host strain to resist certain antimicrobial agents. These plasmids have recently emerged among APEC and they frequently co-transfer with APEC virulence plasmids. Overall, these findings suggest that APEC plasmids are concerning on several levels and pose a serious threat to animal and human health. With this study, we proposed the sequencing of a large APEC resistance plasmid, and subsequent use of the data generated to produce an E. coli plasmid microarray that will be used to scan APEC isolated over the past 35 years for plasmid-associated sequences. During the first year of this study, we have generated a draft sequence of a 3rd APEC virulence plasmid, called p408. The strain harboring this plasmid was selected from a collection of over 1,500 E. coli isolates because it was a typical APEC virulence plasmid in that it possessed a plasmid-encoded PAI, but it was an atypical APEC virulence plasmid in that it also possessed a class 1 integron, a trait not previously identified on such plasmids. This plasmid is currently in the finishing phase, but an initial analysis of p408 revealed that its class 1 integron is inserted in a "hotspot" region which has likely driven the evolution of these colicin-encoding virulence plasmids. We are currently investigating the nature of this site-specific evolution and its implications. In the next year, we will design and create an E. coli plasmid microarray representing all of the coding regions of the 5 avian E. coli plasmids sequenced thus far. We will use this array to examine the plasmid content of APEC and other E. coli isolated during the past 35 years. Additionally, we will perform a transcriptional analysis of the genes represented in this array during infection in the bird. These experiments will shed light on APEC virulence mechanisms and the distribution and/or emergence of APEC plasmids among E. coli populations.

Impacts
This project will aid in determining whether APEC virulence and resistance plasmids are emergent over time. Such results will help to identify future means to control E. coli-caused diseases of birds.

Publications

  • Johnson, T.J., Wannemuehler, Y.M., Johnson, S.J., White, D.G., Doetkott, C., and Nolan, L.K. 2007. Plasmid replicon typing of commensal and pathogenic types of Escherichia coli. Appl. Environ. Microbiol. Epub ahead of print.