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Journal of Bacteriology, November 2000, p. 6272-6276, Vol. 182, No. 21
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
An Escherichia coli Reference Collection
Group B2- and Uropathogen-Associated Polymorphism in the
rpoS-mutS Region of the E. coli
Chromosome
Doreen E.
Culham and
Janet M.
Wood*
Department of Microbiology, University of
Guelph, Guelph, ON N1G 2W1, Canada
Received 8 June 2000/Accepted 10 August 2000
 |
ABSTRACT |
Chromosomal DNAs of enterohemorrhagic, uropathogenic, and
laboratory attenuated Escherichia coli strains differ in
the rpoS-mutS region. Many uropathogens lack a deletion and
an insertion characteristic of enterohemorrhagic strains. At the same
chromosomal position, they harbor a 2.1-kb insertion of unknown origin
with a base composition suggestive of horizontal gene transfer. Unlike
virulence determinants associated with urinary tract infection and/or
neonatal meningitis (pap or prs,
sfa, kps, and hly), the 2.1-kb
insertion is shared by all group B2 strains of the E. coli
Reference Collection.
| |
TEXT |
Genomic sequencing offers
unprecedented opportunities for the identification of genetic
polymorphisms related to bacterial evolution and virulence. The
complete nucleotide sequence of Escherichia coli MG1655
(4), a representative laboratory-attenuated E. coli K-12 strain, provides a foundation for studies of the
evolution and virulence of E. coli strains associated with
diverse pathologies. The expanding list of E. coli virotypes
includes diverse diarrheagenic organisms (labeled enterotoxigenic,
enteropathogenic, enterohemorrhagic, enteroaggregative, enteroinvasive,
and diffusely adherent) (28) as well as isolates associated
with extraintestinal diseases, including neonatal meningitis
(7) and urinary tract infections (UTIs) (including
bacteriuria, cystitis, and pyelonephritis) (11). By
complementing phenotypic analysis and multilocus enzyme
electrophoresis, sequence comparisons are now providing profound
insights into the pathogenesis and evolution of E. coli
(5, 12, 19, 23-25, 28, 29, 37, 39-42). These and other
studies (13, 15) reveal that the chromosomal DNA sequences
of modern organisms reflect both their clonal origins and horizontal
gene transfer.
A uropathogen-associated, rpoS-proximal DNA
polymorphism in E. coli.
Recently, LeClerc et al.
(21) reported that, in comparison to E. coli
MG1655, E. coli O157:H7, related enterohemorrhagic E. coli strains, and Shigella dysenteriae lack 6.1 kb of
chromosomal DNA and harbor a 2.9-kb DNA insertion in the
rpoS-mutS intergenic region (61.5 to 61.7 map units) (Fig.
1). While deleting the rpoS locus from uropathogenic E. coli strains during a study
of osmoregulation and virulence (9, 10), we discovered a
different polymorphism at the same location. E. coli strain
CFT073, a highly virulent isolate from a patient with pyelonephritis
(27), appears to retain the full rpoS-mutS
intergenic sequence characteristic of E. coli MG1655
(Fig. 1). In addition, a 2.1-kb DNA insert replaces the 2.9-kb
sequence identified by LeClerc et al. (21). This insert was
initially detected when attempts to PCR amplify rpoS failed
to produce a DNA fragment of the expected size (primers A and G) (Fig.
2). Genomic DNA from E. coli
CFT073 was prepared as follows (36). Bacteria harvested from
a 1-ml overnight culture in Luria-Bertani medium (26) were
washed once with 1 ml of saline (0.85% [wt/vol] NaCl), resuspended
in 0.5 ml of distilled water, boiled for 10 min, and chilled on ice.
Debris was removed by centrifugation, and the relevant sequences were
PCR amplified with 5 µl of the resulting extract as a template
(8). The insert sequence was determined by GenAlyTiC
(University of Guelph, Guelph, Ontario). Additional primers were
created as required to complete this 2.1-kb sequence (Fig. 2). The
inserted DNA occurs at exactly the same location as that present in
E. coli O157:H7 but differs in both size and sequence (the
insert sequences are not related). It has a base composition of 40%
G+C, a value much lower than the average for E. coli
K-12 (50%) and for the immediately flanking sequences (52%). The
insert may therefore have arrived in E. coli by horizontal gene transfer (29).
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FIG. 1.
Comparison of the rpoS-mutS intergenic
regions of E. coli K-12 (laboratory) (4),
E. coli CFT073 (pyelonephritis) (this study), and E. coli O157:H7 (hemorrhagic colitis) (21). E. coli CFT073 lacks the 6.1-kb DNA deletion in the
rpoS-mutS intergenic region that is characteristic of
enterohemorrhagic strains (e.g., O157:H7). However the presence of the
full 6.1-kb rpoS-mutS intergenic sequence found in E. coli MG1655 has not been verified for E. coli CFT073.
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FIG. 2.
The rpoS-mutS intergenic region of E. coli CFT073 (accession no. AF270497) and its detection by PCR
amplification. (A) Physical map, showing positions of ORFs (Table 2)
and locations of DNA fragments amplified by PCR (Tables 1 and 3). (B)
PCR primers used to perform the multiplex PCR analyses reported in
Tables 1 and 3.
|
|
To determine the distribution of the inserted sequence, we applied PCR
analysis to chromosomal DNA isolated from diverse clinical
E. coli isolates (Table
1). DNA was
prepared (
36), and PCR
was performed (
8) using
the primers listed in Table
1 and
Fig.
2B (two pairs of primers per
PCR). Production of a 301-bp
amplicon during test 1 (primers C and D)
indicated the presence
of the inserted sequence. Production of 579- (primers E and F)
and 483-bp (primers A and B) amplicons during test 2 indicated
its location in the
rpoS-mutS region. PCR
amplification of the
housekeeping locus
putP, located at
23.3 map units, provided a
positive control for the quality of the DNA
templates. A DNA insert
similar to that discovered in pyelonephritis
isolate CFT073 was
present in a majority of UTI isolates, including
bacteria isolated
from patients with uncomplicated pyelonephritis (7 of
7) or cystitis
(8 of 12) and unspecified UTIs (4 of 4). It was present
in approximately
one-half of the tested isolates from patients with
catheter-associated
infections (3 of 7), and it was uncommon among
bacteria isolated
from patients with hemorrhagic colitis (0 of 5) or
infantile diarrhea
(2 of 21). When present, it was located in the
rpoS-mutS region
(Table
1).
No 301-bp PCR product (internal to the DNA insert) was observed when
PCR test 1 was applied with chromosomal DNA from
Salmonella enterica serovar Typhimurium,
Klebsiella oxytoca,
Pseudomonas putida,
Pseudomonas paucimobilis,
Vibrio anguillarum,
Yersinia ruckeri,
Erwinia carotovora,
Hafnia alvei,
Enterobacter cloacae,
or
S. dysenteriae as a
template. Like that from some
E. coli isolates
listed in
Table
1, chromosomal DNA from
S. dysenteriae supported
DNA
amplification with PCR test 2, but the resulting pattern of
DNA
fragments differed from that observed with
E. coli CFT073
DNA as a template. Thus, the DNA insert observed in
E. coli
CFT073
was different from that found in
E. coli O157:H7 and
S. dysenteriae type 1 (
21). It was more common
among UTI isolates than among
the other clinical
E. coli
isolates included in this study, and
it was not detected by PCR
amplification in an array of other
organisms.
Analysis of the DNA sequence inserted in
E. coli CFT073
revealed two open reading frames (ORFs) encoding proteins greater
than
10 kDa in molecular mass for which similar sequences could
be found
(Fig.
2 and Table
2). ORF183 showed 26%
identity to
WrbA, a flavodoxinlike protein that is expressed by
E. coli K-12
during stationary phase and whose sequence
homologues have been
found in bacteria, yeast, and plants
(
14). ORF347 showed comparable,
limited levels of similarity
to enzymes implicated in antibiotic
hydrolysis (
1) and
synthesis (
2). Though the base composition
of the DNA
encoding ORF183 was similar to that of
E. coli K-12
(49%),
the base composition of the DNA encoding ORF347 was much
lower (39%),
suggesting that they may differ in origin. No sequence
similarity was
sufficiently high to suggest the recent transfer
of the entire 2.1-kb
sequence or its subfragments from another
organism.
The inserted sequence is present in all members of the ECOR group
B2.
The E. coli Reference (ECOR) Collection, a set of
E. coli strains isolated from diverse hosts and geographic
locations, was designed to represent the variation and genetic
structure of E. coli (30). Studies of
housekeeping loci, applied to these strains and others, clearly define
the clonal nature of natural E. coli populations (18,
40). We explored the evolutionary origin of the 2.1-kb
rpoS-proximal inserted sequence by examining its occurrence
among the 72 ECOR strains (Table 3). PCR
test 1 (Table 1) detected this sequence in ECOR strains EC23 and EC32
and in each of the ECOR group B2 strains. UTI-related virulence
determinants, believed to have arrived by horizontal gene transfer,
occur at higher frequency within ECOR group B2 than among other ECOR
strains (Table 3) (6, 20, 22). The presence of the
rpoS-proximal 2.1-kb insertion within group B2 members is
therefore consistent with its presence in many UTI isolates (Table 1).
This insertion is present in all group B2 isolates, whereas few contain
all of the tested UTI-linked virulence determinants (pap,
prs, sfa, kps, and hly),
each of which varies in chromosome map position among E. coli isolates. It is thus likely that the 2.1-kb insertion arrived
earlier than these virulence determinants during the evolution of group
B2.
Some data suggest that genomic sequences common to group B2 organisms
diverge deeply from those of commensal
E. coli strains
in
ECOR groups A and B1 and have provided an essential context
for the
evolution of extraintestinal virulence (
3,
32). Bingen
et
al. compared the distribution of ribotypes and virulence markers
associated with extraintestinal infections for 69 neonatal meningitis
isolates and for the ECOR strains (
3). The neonatal
meningitis
isolates were concentrated in phylogenetic group B2. Though
present
in all phylogenetic groups, virulence markers linked to
neonatal
meningitis (including
sfa or
foc and
ibe-10) were also present
at the highest frequency in group
B2. In contrast, the UTI-associated
marker
pap was present
at the highest frequencies in non-B2 neonatal
meningitis isolates and
in group B2 ECOR strains. The 2.1-kb
rpoS-proximal
DNA
insertion present in group B2 ECOR strains and many uropathogens
was
not detected in the single neonatal meningitis isolate included
in this
study (Table
1). Given their concentration in group B2,
the 2.1-kb
sequence may be found within other neonatal meningitis
isolates.
Nucleotide sequence accession number.
The 2.1-kb insert in the
rpoS-mutS intergenic region of E. coli CFT073 was
registered with GenBank under accession no AF270497.
| |
ACKNOWLEDGMENTS |
We are grateful to R. M. W. Stevenson for chromosomal
DNAs isolated from diverse bacteria, to C. Whitfield and Karen Amor for
chromosomal DNA isolated from the ECOR strains, and to C. L. Gyles
for S. dysenteriae and for comments on the manuscript.
We thank the Medical Research Council of Canada for Research Operating
Grant MT-15113.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, University of Guelph, Guelph, ON N1G 2W1, Canada. Phone: (519) 824-4120 ext. 3866. Fax: (519) 837-1802. E-mail:
jwood{at}uoguelph.ca.
| |
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Journal of Bacteriology, November 2000, p. 6272-6276, Vol. 182, No. 21
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Hengge-Aronis, R.
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Kotewicz, M. L., Li, B., Levy, D. D., LeClerc, J. E., Shifflet, A. W., Cebula, T. A.
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Culham, D. E., Lu, A., Jishage, M., Krogfelt, K. A., Ishihama, A., Wood, J. M.
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Brown, E. W., LeClerc, J. E., Li, B., Payne, W. L., Cebula, T. A.
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