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Journal of Clinical Microbiology, January 2001, p. 14-23, Vol. 39, No. 1
Wellcome Trust Centre for the Epidemiology of
Infectious Disease, Department of Zoology, University of Oxford, Oxford
OX1 3FY,1 The Public Health Laboratory,
Royal Preston Hospital, Preston PR2 9HG,2
and The Public Health Laboratory, Withington Hospital,
Manchester M20 8LR,3 United Kingdom, and
Research Laboratory for Infectious Diseases, National Institute
of Public Health and the Environment, 3720 BA Bilthoven, The
Netherlands4
Received 20 June 2000/Returned for modification 4 September
2000/Accepted 16 October 2000
The gram-negative bacterium Campylobacter jejuni has
extensive reservoirs in livestock and the environment and is a frequent cause of gastroenteritis in humans. To date, the lack of (i) methods suitable for population genetic analysis and (ii) a universally accepted nomenclature has hindered studies of the epidemiology and
population biology of this organism. Here, a multilocus sequence typing
(MLST) system for this organism is described, which exploits the
genetic variation present in seven housekeeping loci to determine the
genetic relationships among isolates. The MLST system was established
using 194 C. jejuni isolates of diverse origins, from humans, animals, and the environment. The allelic profiles, or sequence
types (STs), of these isolates were deposited on the Internet
(http://mlst.zoo.ox.ac.uk), forming a virtual isolate collection which
could be continually expanded. These data indicated that C. jejuni is genetically diverse, with a weakly clonal population structure, and that intra- and interspecies horizontal genetic exchange
was common. Of the 155 STs observed, 51 (26% of the isolate collection) were unique, with the remainder of the collection being
categorized into 11 lineages or clonal complexes of related STs with
between 2 and 56 members. In some cases membership in a given lineage
or ST correlated with the possession of a particular Penner HS
serotype. Application of this approach to further isolate collections
will enable an integrated global picture of C. jejuni epidemiology to be established and will permit more detailed studies of
the population genetics of this organism.
Campylobacter jejuni is
the most common causative agent of human enterocolitits in many
industrialized countries, representing a substantial drain on public
health resources. Typically, infection is associated with sudden onset
of fever, abdominal cramps, and diarrhea containing blood and
leukocytes (16, 30, 34). Sequelae occur occasionally, and
links have been made between infection by particular C. jejuni serotypes and Guillain-Barré syndrome (24). The gram-negative bacterium is widespread in the
environment (13), forming part of the natural intestinal
flora of birds and mammals (17). The handling or
consumption of raw or undercooked meat products, particularly chicken
contaminated during slaughter, is often implicated in disease
(3). However, the majority of C. jejuni
infections are considered to be sporadic, with the source of infection
remaining unidentified (2). Occasional larger-scale outbreaks of campylobacteriosis have been linked with consumption of
contaminated water or raw milk (17, 27).
A plethora of methods have been developed to discriminate C. jejuni isolates for the investigation of epidemiology and
infections. However, the lack of widely available reagents for methods
such as serotyping has limited their general use. Genotyping methods have been developed (36), but the techniques and their
interpretation have not been standardized or broadly accepted. This,
coupled with the lack of a universal nomenclature system for isolate
profiles, has prevented the development of an international
campylobacter typing database.
Multilocus sequence typing (MLST) (20) has been successful
in the characterization of several other bacteria (1, 8, 20,
33). This technique employs the same philosophy as multilocus enzyme electrophoresis (29), in that neutral genetic
variation from multiple chromosomal locations is indexed, but exploits
nucleotide sequence determination to identify this variation. In MLST
studies of other bacteria, stretches of nucleotide sequence of ~500
bp from 7 loci provided discrimination approximately equivalent to that
obtained with 15 to 20 loci in multilocus enzyme electrophoresis analyses (20). Sequence data are readily compared among
laboratories and lend themselves to electronic storage and
distribution. Furthermore, MLST can reduce the need to transport live
bacteria, since nucleotide sequence determination from PCR products can
be achieved from killed-cell suspensions, purified DNA, or clinical
material. A World Wide Web site for the storage and exchange of data
and protocols for MLST has been established (http://mlst.zoo.ox.ac.uk).
While MLST is particularly suited to long-term and global epidemiology, as it identifies variation which is accumulating slowly within a
population (20), the data can be used in the investigation of individual outbreaks, especially when MLST data are combined with
other data, such as the nucleotide sequences of genes encoding antigens
(6, 9).
Here, an MLST scheme for C. jejuni is described. The system
is based on the nucleotide sequences of seven housekeeping loci and was
established by the examination of 194 isolates obtained from a variety
of sources. A total of 155 distinct sequence types (STs) were
identified, which were resolved into 62 clonal lineages or complexes.
There was evidence for extensive horizontal genetic exchange, including
import of alleles from at least two other Campylobacter
species, including C. coli. Further analysis indicated that
C. jejuni had a weakly clonal population structure and that some complexes were associated with particular Penner HS serotypes. These results provide a basis for further investigations of the epidemiology and population genetics of C. jejuni by MLST.
Campylobacter isolates.
C. jejuni isolates were
obtained from the collection held at Preston Public Health Laboratory,
Preston, United Kingdom (35), and included isolates from
cases of human campylobacteriosis, livestock, and the environment.
Reference isolates for the Penner heat-stable antigen serotyping scheme
(28) were donated to the Preston Public Health Laboratory
culture collection by J. Penner and are available from the National
Collection of Type Cultures and American Type Culture Collection.
Eleven further isolates were obtained from a collection held in The
Netherlands at the Research Laboratory for Infectious Diseases, at the
National Institute of Public Health and the Environment, and at the
Department of Bacteriology, Institute for Animal Science and Health. Of
these, the nonhuman isolates were obtained from geographically
dispersed farms in The Netherlands (11), and human
isolates were obtained from a case-control study among general
practitioners in The Netherlands. The total of 194 isolates comprised
79 from human cases of campylobacteriosis, 38 from livestock, 34 from
environmental locations, 3 from milk, and 40 of the reference isolates
for the Penner serotyping scheme. Of the human isolates, 75 were from
cases which occurred in the United Kingdom during 1990 and 1991, 3 were
isolated in the Netherlands during 1997 and 1998, and 1 was obtained
from a case in Australia during 1998. The livestock isolates included
34 from chickens, 3 from cattle, and 1 from a duck (including 24 isolates from the United Kingdom, 5 from The Netherlands, and 5 from
New Zealand, all isolated during the 1990s). The three isolates from
milk were obtained in the United Kingdom during 1991, and all of the
environmental isolates were from the sand of bathing beaches (United
Kingdom, 1994 and 5), with the exception of one, which was from water
(United Kingdom, 1991).
Culture of isolates and preparation of chromosomal DNA.
All
of the bacterial isolates included had been maintained with minimal
passages at Choice of loci.
A number of candidate loci, encoding enzymes
responsible for intermediary metabolism, were identified by searching
the C. jejuni genome database
(http://www.sanger.ac.uk/Projects/C_jejuni/) (26) with gene
sequences from other bacteria. Suitable genes were then chosen on the
basis of a number of criteria, including chromosomal location,
suitability for primer design, and sequence diversity in pilot studies.
The following seven loci were chosen for the MLST scheme (protein
products are shown in parentheses): aspA (aspartase A),
glnA (glutamine synthetase), gltA (citrate synthase), glyA (serine hydroxymethyltransferase),
pgm (phosphoglucomutase), tkt (transketolase),
and uncA (ATP synthase
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.1.14-23.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Multilocus Sequence Typing System for
Campylobacter jejuni
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
70°C in 20% (vol/vol) glycerol in brain heart infusion
broth, and consequently none of the genetic variation studied was
likely to have been introduced during storage. Prior to DNA extraction,
cultures were removed from storage and allowed to thaw at room
temperature. For each isolate, a blood agar plate was spread for
discrete colonies and incubated at 37°C for 72 h under
microaerobic conditions (5). Chromosomal DNA was extracted using an Isoquick kit (Microprobe Corporation) or Wizard genomic DNA
purification kit (Promega, Madison, Wis.).
subunit). The chromosomal locations of these housekeeping loci suggested that it was unlikely for
any of them to be coinherited in the same recombination event, as the
minimum distance between loci was 70 kb (Fig.
1).
View larger version (19K):
[in a new window]
FIG. 1.
Chromosomal locations of MLST loci. The positions of the
seven loci are shown on a map of the C. jejuni chromosome
derived from the genome sequence of isolate NCTC 11168 (http://www.sanger.ac.uk/Projects/C_jejuni/). The 1,641,481-bp genome is
divided into 10 segments (indicated on the inner circle), with each
segment representing 164,148 bp.
Amplification and nucleotide sequence determination.
PCR
products were amplified with oligonucleotide primer pairs designed from
the published C. jejuni sequence (26). A range of primers were tested, with those shown in Table
1 providing reliable amplification from a
diverse range of samples (additional dideoxyoligonucleotide primers are
described at http://mlst.zoo.ox.ac.uk). Each 50-µl amplification
reaction mixture comprised ~10 ng of campylobacter chromosomal DNA, 1 µM each PCR primer, 1× PCR buffer (Perkin-Elmer Corp.), 1.5 mM
MgCl2, 0.8 mM deoxynucleoside triphosphates, and 1.25 U of
Amplitaq polymerase (Perkin-Elmer Corp.). The reaction conditions were
denaturation at 94°C for 2 min, primer annealing at 50°C for 1 min,
and extension at 72°C for 1 min, for 35 cycles. The amplification
products were purified by precipitation with 20% polyethylene
glycol-2.5 M NaCl (7), and their nucleotide sequences
were determined at least once on each DNA strand using internal nested
primers (Table 1) and BigDye Ready Reaction Mix (PE Biosystems) in
accordance with the manufacturer's instructions. Unincorporated dye
terminators were removed by precipitation of the termination products
with 95% ethanol, and the reaction products were separated and
detected with an ABI Prism 3700 or an ABI Prism 377 automated DNA
sequencer (PE Biosystems). Sequences were assembled from the resultant
chromatograms with the STADEN suite of computer programs
(32).
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Allele and ST assignment. For each locus, distinct allele sequences were assigned arbitrary allele numbers in order of identification; these were in-frame internal fragments of the gene which contained an exact number of codons. Each isolate was therefore designated by seven numbers, constituting an allelic profile or ST. The data were deposited in a database accessible on the Internet at http://mlst.zoo.ox.ac.uk/. The STs were identified by arbitrary numbers assigned in order of description (e.g., ST-1). New sequences were assigned allele numbers and isolates were assigned their STs by interrogating the database. Allele numbers for new sequences and ST numbers for new allelic profiles are available by submission to the database.
The STs were grouped into lineages or clonal complexes using the program BURST (E. J. Feil and M.-S. Chan, available at http://mlst.zoo.ox.ac.uk). The members of a lineage were defined as groups of two or more independent isolates with an ST that shared identical alleles at four or more loci. Each lineage was named after the ST identified as the putative founder of the group by BURST, followed by the word "complex" (e.g., ST-21 complex).Phylogenetic analyses. The degree of clonality within the data set was estimated by measuring the index of association (IA) and was calculated for all STs and for a subset of STs representative of each lineage with a program written by J. Maynard Smith (23). The relationships among the STs in a given complex were investigated by constructing a distance matrix of allelic mismatches with the program MLD DISTANCE MATRIX (K. A. Jolley). Each locus difference was treated identically in that no relationships among the different alleles were assumed. The distance matrix was then visualized by Split decomposition analysis using SPLITSTREE version 3.1 (14, 21). Where necessary, higher resolution of the splits graph was obtained by progressively pruning resolved branches, and the graphs were annotated by reference to the allelic profiles. Other data analyses, including calculation of dN/dS, were performed using the MEGA suite of programs (18). All of the programs were available for electronic downloading (http://mlst.zoo.ox.ac.uk, http://bibserv.techfak.uni-bielefeld.de/splits, and http://evolgen.biol.metro-u.ac.jp/MEGA/).
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RESULTS |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Diversity of housekeeping genes.
The alleles defined for the
MLST scheme were between 402 bp (gltA) and 507 bp
(glyA) in length, and between 27 (gltA and
unc) and 46 (pgm) alleles were present per locus.
The proportion of variable sites present in the MLST alleles ranged
from 9.2% (pgm) to 21.2% (tkt). In part, this
was due to the polymorphisms present in a minority of alleles which
were divergent (11 to 15% nucleotide sequence difference) from all
other allele sequences. Such alleles were observed at least once for
each of the MLST loci and were present in a total of 11 isolates, which
had divergent alleles at between one and six loci. Searches of the
GenBank database established that two of these, at the gltA
locus, were very similar (97% nucleotide sequence identity) to the
sequence of this gene from C. coli. When the divergent
alleles were removed from analysis, the remaining allele sequences had
between 5.2% (aspA) and 11.8% (pgm) variable
sites (Table 2).
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STs and lineages.
There were a total of 155 STs among the 194 isolates examined, 140 (90%) of which were present only once, with the
most common ST (ST-21) occurring eight times in the dataset. Assignment
of the STs to lineages established that 51 STs were both unique and unrelated to any others (data are available at
http://mlst.zoo.ox.ac.uk/). The remaining isolates were assigned to 11 complexes: the ST-21 complex was the largest, with 56 members; the
ST-45 complex had 23 members; and the ST-179 complex comprised 7 STs.
There were two lineages with three member STs (two lineages) and six
lineages with two members (Table 3). The
IA for the complete data set was
2.016, with a value of 0.5671 obtained when only one
representative of each lineage was included.
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Interrelationships of members of the ST-21 complex.
The
relationships among members of the ST-21 complex were visualized by an
annotated splits graph of a distance matrix generated by pairwise
comparisons of the allelic profiles (Fig.
3). The unresolved splits graph including
all members of the complex is shown at the top left of Fig. 3. The
outer branches were then pruned to show a partially resolved network,
which was further pruned to resolve completely the center of the graph.
Consistent with the lineage assignment by BURST, this placed the
predicted founder ST at a central position of the split graph. The
relationships among other members of the group were assessed by
examining the number of nodes (representing the number of changes)
between two isolates. For example, in the central region of the graph,
ST-21 and ST-19 are separated by one node, representing one allele
change between the two. Their STs are 2-1-1-3-2-1-5 and 2-1-5-3-2-1-5, respectively. ST-21 and ST-31 were separated by two nodes and differed
by two alleles (ST-31 is 2-20-12-3-2-1-5).
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Relationships of lineage, source, and serotype. Isolates belonging to the two largest lineages present in the data set, the ST-21 complex and ST-45 complex, had originated from a diversity of sources (Table 3). The ST-21 complex included 59 of the 79 human isolates studied (75%), 14 of the 34 chicken isolates (41%), 7 of the 33 sand isolates (21%), 3 of the 3 cattle isolates (100%), and 3 of the 3 milk isolates (100%). The ST-45 complex included 10 of the 79 human isolates (13%), 11 of the 34 chicken isolates (32%), and 2 of the 33 sand isolates (6%). Three Penner HS serotypes predominated in the ST-21 complex (HS1, 25%; HS2, 33%; and HS4, 8%), and some of the STs forming this lineage were homogenous for serotype (e.g., the six ST-19 isolates were all HS1, while the eight ST-21 isolates were all HS2 or non typeable), although these serotypes were also present in isolates exhibiting different STs. Conversely, the ST-45 complex contained a wide variety of serotypes and a number of cross-reactive isolates, but the two most common serotypes observed in the ST-21 complex, HS1 and HS2, were not present in the ST-45 complex. The remaining complexes comprised small numbers in the isolate collection and these were homogenous for serotype, with the exception of the seven ST-179 complex isolates which originated in sand and were HS2 or HS5 and two members of the ST-130 complex (Table 3).
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DISCUSSION |
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Abstract
Introduction
Materials and Methods
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Discussion
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Unambiguous, discriminatory isolate characterization schemes are essential for epidemiological, population genetic, and evolutionary studies. Ideally, these schemes generate data that are relevant to all of these areas, but before the recent advent of high-throughput nucleotide sequence determination technology, this goal had proved elusive (19). There is a particular need for appropriate typing schemes for C. jejuni, as this common human pathogen (3) has extensive animal and environmental reservoirs and the relationships between disease-associated and animal or environmental populations remain to be fully elucidated. This study demonstrates that MLST (i) discriminates among C. jejuni isolates effectively and (ii) generates data that can be applied to the investigation of the population structure and evolutionary mechanisms in this organism. The advantages of MLST include high discrimination, reproducibility, simplicity of interpretation by using one technique rather than a combination of techniques, and the generation of data which are directly comparable among laboratories via the Internet (20). The ease with which the system can be transferred among laboratories was exploited in this study, with the sequence determinations being performed in two separate locations (Oxford and Bilthoven).
The seven loci chosen were a suitable basis for an MLST typing scheme, as they could be amplified and sequenced from isolates obtained from a wide variety of sources, were unlinked on the C. jejuni chromosome (Fig. 1), exhibited sufficient diversity to provide a high degree of resolution, and were not subject to positive selection, as demonstrated by the dN/dS ratios calculated for each locus (Table 2). The fact that the dN/dS ratios were much less than 1 demonstrates that there is selection against amino acid change (a dN/dS ratio of greater than 1 implies selection for amino acid changes). The nucleotide sequence determination for these loci was consistent with the results obtained previously from a number of phenotypic and genotypic studies of C. jejuni, which suggested that populations of this organism are highly diverse (35, 36). Some of this diversity was likely to have been imported recently from related species, with a potential donor, C. coli, identified for some of the more diverse sequences. When these likely importation events were excluded (Table 2), the C. jejuni sample exhibited nucleotide sequence diversity similar to that observed in Neisseria meningitidis (12, 15a, 20) and substantially greater than that seen in Streptococcus pneumoniae (8).
The housekeeping gene sequences provided evidence that horizontal genetic exchange has a major influence on the structure and evolution of Campylobacter populations, which was itself consistent with previous findings for the antigen genes of C. jejuni (10). The fall in the IA from 2, for the whole data set, to 0.57, when only one example of each lineage was included, was indicative of a weakly clonal population (22) which contained a number of clonal complexes of relatively recent evolutionary origin with no tree-like phylogenetic relationship with each other (12). The presence of the same allele in isolates of diverse origins and different lineages (for example, aspA allele number 2 in isolates from humans, sand, and poultry) supported this view, as did the fact that the majority of changes within the most common lineages were likely to be due to recombinational replacement rather than mutation.
The presence of apparent lineages in isolate collections of weakly clonal organisms may be amplified by sampling (23); for example, the presence of many isolates belonging to the ST-21 complex could have been a consequence of members of this complex being more likely to be associated with human infection. Alternatively, certain lineages might be associated with a particular niche, for example, the ST-179 complex, which contained environmental isolates (from sand of United Kingdom bathing beaches) (4). Further MLST analyses of appropriate isolate collections are necessary to address these questions more fully. However, the finding that human isolates cluster predominantly in the ST-21 complex, while chicken isolates have a broader distribution, suggests that it may be unlikely that the majority of the human strains come from chickens but that human strains may come from different sources like cattle, although the number of strains studied from cattle were low. A more detailed nucleotide sequence-based investigation of the relationships of organisms classified as different Campylobacter species is also warranted given the evidence for genetic exchange among these organisms.
A number of typing techniques have been applied to C. jejuni, with Penner HS typing, which is based on the lipopolysaccharide component of the outer membrane (28), being favored by many laboratories. The data presented here demonstrated that the Penner HS serotype was consistent and conserved in some lineages, (Table 3); for example, there was a correlation between Penner HS type and ST among some members of the ST-21 complex. However, the members of the ST-45 complex were highly diverse for Penner HS serotype (Table 3). These data are consistent with those reported earlier (25, 31, 35) and suggested the existence of a number of C. jejuni strains which were genetically and antigenically stable over the sampling period.
This data set provides a basis for the exploitation of MLST in the study of C. jejuni. The MLST approach is in principle applicable to any bacterial species, and while the oligonucleotide primers described here were not designed for characterization of other Campylobacter species, the evidence for interspecies horizontal genetic exchange between C. jejuni and at least one other Campylobacter species strongly suggests that this MLST system will be directly applicable to other Campylobacter species. The identification of alleles with gene sequences that were diverse from the majority of C. jejuni sequences may indicate disparity between microbiological and nucleotide sequence-based species classifications of these organisms, but additional data and analyses will be required to address these issues.
The MLST scheme provides a means for the investigation of disease outbreaks in both global and local contexts, permitting confirmation of suspected routes of transmission from the environment and livestock to humans. In addition, MLST data will assist in resolving broader issues such as the relationship of environmental to disease isolates at the population level, the structure of Campylobacter populations, the existence or otherwise of widely distributed lineages, and the extent of intra- and interspecies recombination. The Campylobacter MLST website is a freely accessible resource available to the community as a whole for the investigation of this important and as yet incompletely understood pathogen. Submission of data from other laboratories is welcomed.
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ACKNOWLEDGMENTS |
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This work was funded by the United Kingdom Ministry of Agriculture, Fisheries and Food (contract number OZ0604).
We are grateful to Birgitta Duim and Jaap Wagenaar, Department of Bacteriology, Institute for Animal Science and Health, Lelystad, The Netherlands, for providing the chromosomal DNA of the human and animal campylobacter isolates from The Netherlands.
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FOOTNOTES |
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* Corresponding author. Mailing address: Wellcome Trust Centre for the Epidemiology of Infectious Disease, Department of Zoology, University of Oxford, South Parks Rd., Oxford OX1 3FY, United Kingdom. Phone: [44] (1865) 271284. Fax: [44] (1865) 271284. E-mail: martin.maiden{at}zoo.ox.ac.uk.
Present address: Department of Microbiology and Immunology, UCLA
School of Medicine, Los Angeles, CA 90095-1747.
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Discussion
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Journal of Clinical Microbiology, January 2001, p. 14-23, Vol. 39, No. 1
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.1.14-23.2001
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(2005). Effects of Subtherapeutic Administration of Antimicrobial Agents to Beef Cattle on the Prevalence of Antimicrobial Resistance in Campylobacter jejuni and Campylobacter hyointestinalis. Appl. Environ. Microbiol.
71: 3872-3881
[Abstract] [Full Text] -
Schouls, L. M., van der Ende, A., van de Pol, I., Schot, C., Spanjaard, L., Vauterin, P., Wilderbeek, D., Witteveen, S.
(2005). Increase in Genetic Diversity of Haemophilus influenzae Serotype b (Hib) Strains after Introduction of Hib Vaccination in The Netherlands. J. Clin. Microbiol.
43: 2741-2749
[Abstract] [Full Text] -
Clark, C. G., Bryden, L., Cuff, W. R., Johnson, P. L., Jamieson, F., Ciebin, B., Wang, G.
(2005). Use of the Oxford Multilocus Sequence Typing Protocol and Sequencing of the Flagellin Short Variable Region To Characterize Isolates from a Large Outbreak of Waterborne Campylobacter sp. Strains in Walkerton, Ontario, Canada. J. Clin. Microbiol.
43: 2080-2091
[Abstract] [Full Text] -
Miller, W. G., On, S. L. W., Wang, G., Fontanoz, S., Lastovica, A. J., Mandrell, R. E.
(2005). Extended Multilocus Sequence Typing System for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus. J. Clin. Microbiol.
43: 2315-2329
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Nemoy, L. L., Kotetishvili, M., Tigno, J., Keefer-Norris, A., Harris, A. D., Perencevich, E. N., Johnson, J. A., Torpey, D., Sulakvelidze, A., Morris, J. G. Jr., Stine, O. C.
(2005). Multilocus Sequence Typing versus Pulsed-Field Gel Electrophoresis for Characterization of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli Isolates. J. Clin. Microbiol.
43: 1776-1781
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Dingle, K. E., Colles, F. M., Falush, D., Maiden, M. C. J.
(2005). Sequence Typing and Comparison of Population Biology of Campylobacter coli and Campylobacter jejuni. J. Clin. Microbiol.
43: 340-347
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de las Rivas, B., Marcobal, A., Munoz, R.
(2004). Allelic Diversity and Population Structure in Oenococcus oeni as Determined from Sequence Analysis of Housekeeping Genes. Appl. Environ. Microbiol.
70: 7210-7219
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Klena, J. D., Parker, C. T., Knibb, K., Ibbitt, J. C., Devane, P. M. L., Horn, S. T., Miller, W. G., Konkel, M. E.
(2004). Differentiation of Campylobacter coli, Campylobacter jejuni, Campylobacter lari, and Campylobacter upsaliensis by a Multiplex PCR Developed from the Nucleotide Sequence of the Lipid A Gene lpxA. J. Clin. Microbiol.
42: 5549-5557
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Brown, P. E., Christensen, O. F., Clough, H. E., Diggle, P. J., Hart, C. A., Hazel, S., Kemp, R., Leatherbarrow, A. J. H., Moore, A., Sutherst, J., Turner, J., Williams, N. J., Wright, E. J., French, N. P.
(2004). Frequency and Spatial Distribution of Environmental Campylobacter spp.. Appl. Environ. Microbiol.
70: 6501-6511
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Taboada, E. N., Acedillo, R. R., Carrillo, C. D., Findlay, W. A., Medeiros, D. T., Mykytczuk, O. L., Roberts, M. J., Valencia, C. A., Farber, J. M., Nash, J. H. E.
(2004). Large-Scale Comparative Genomics Meta-Analysis of Campylobacter jejuni Isolates Reveals Low Level of Genome Plasticity. J. Clin. Microbiol.
42: 4566-4576
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Mellmann, A., Mosters, J., Bartelt, E., Roggentin, P., Ammon, A., Friedrich, A. W., Karch, H., Harmsen, D.
(2004). Sequence-Based Typing of flaB Is a More Stable Screening Tool Than Typing of flaA for Monitoring of Campylobacter Populations. J. Clin. Microbiol.
42: 4840-4842
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Cladera, A. M., Bennasar, A., Barcelo, M., Lalucat, J., Garcia-Valdes, E.
(2004). Comparative Genetic Diversity of Pseudomonas stutzeri Genomovars, Clonal Structure, and Phylogeny of the Species. J. Bacteriol.
186: 5239-5248
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Schouls, L. M., van der Heide, H. G. J., Vauterin, L., Vauterin, P., Mooi, F. R.
(2004). Multiple-Locus Variable-Number Tandem Repeat Analysis of Dutch Bordetella pertussis Strains Reveals Rapid Genetic Changes with Clonal Expansion during the Late 1990s. J. Bacteriol.
186: 5496-5505
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Connerton, P. L., Loc Carrillo, C. M., Swift, C., Dillon, E., Scott, A., Rees, C. E. D., Dodd, C. E. R., Frost, J., Connerton, I. F.
(2004). Longitudinal Study of Campylobacter jejuni Bacteriophages and Their Hosts from Broiler Chickens. Appl. Environ. Microbiol.
70: 3877-3883
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Best, E. L., Fox, A. J., Frost, J. A., Bolton, F. J.
(2004). Identification of Campylobacter jejuni Multilocus Sequence Type ST-21 Clonal Complex by Single-Nucleotide Polymorphism Analysis. J. Clin. Microbiol.
42: 2836-2839
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Konkel, M. E., Klena, J. D., Rivera-Amill, V., Monteville, M. R., Biswas, D., Raphael, B., Mickelson, J.
(2004). Secretion of Virulence Proteins from Campylobacter jejuni Is Dependent on a Functional Flagellar Export Apparatus. J. Bacteriol.
186: 3296-3303
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Feil, E. J., Li, B. C., Aanensen, D. M., Hanage, W. P., Spratt, B. G.
(2004). eBURST: Inferring Patterns of Evolutionary Descent among Clusters of Related Bacterial Genotypes from Multilocus Sequence Typing Data. J. Bacteriol.
186: 1518-1530
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Helgason, E., Tourasse, N. J., Meisal, R., Caugant, D. A., Kolsto, A.-B.
(2004). Multilocus Sequence Typing Scheme for Bacteria of the Bacillus cereus Group. Appl. Environ. Microbiol.
70: 191-201
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Hopkins, K. L., Desai, M., Frost, J. A., Stanley, J., Logan, J. M. J.
(2004). Fluorescent Amplified Fragment Length Polymorphism Genotyping of Campylobacter jejuni and Campylobacter coli Strains and Its Relationship with Host Specificity, Serotyping, and Phage Typing. J. Clin. Microbiol.
42: 229-235
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Colles, F. M., Jones, K., Harding, R. M., Maiden, M. C. J.
(2003). Genetic Diversity of Campylobacter jejuni Isolates from Farm Animals and the Farm Environment. Appl. Environ. Microbiol.
69: 7409-7413
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Duim, B., Godschalk, P. C. R., van den Braak, N., Dingle, K. E., Dijkstra, J. R., Leyde, E., van der Plas, J., Colles, F. M., Endtz, H. P., Wagenaar, J. A., Maiden, M. C. J., van Belkum, A.
(2003). Molecular Evidence for Dissemination of Unique Campylobacter jejuni Clones in Curacao, Netherlands Antilles. J. Clin. Microbiol.
41: 5593-5597
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Dodgson, A. R., Pujol, C., Denning, D. W., Soll, D. R., Fox, A. J.
(2003). Multilocus Sequence Typing of Candida glabrata Reveals Geographically Enriched Clades. J. Clin. Microbiol.
41: 5709-5717
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Manning, G., Dowson, C. G., Bagnall, M. C., Ahmed, I. H., West, M., Newell, D. G.
(2003). Multilocus Sequence Typing for Comparison of Veterinary and Human Isolates of Campylobacter jejuni. Appl. Environ. Microbiol.
69: 6370-6379
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Ko, K. S., Hong, S. K., Lee, H. K., Park, M.-Y., Kook, Y.-H.
(2003). Molecular Evolution of the dotA Gene in Legionella pneumophila. J. Bacteriol.
185: 6269-6277
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Wang, X.-M., Noble, L., Kreiswirth, B. N., Eisner, W., McClements, W., Jansen, K. U., Anderson, A. S.
(2003). Evaluation of a multilocus sequence typing system for Staphylococcus epidermidis. J Med Microbiol
52: 989-998
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Sails, A. D., Swaminathan, B., Fields, P. I.
(2003). Utility of Multilocus Sequence Typing as an Epidemiological Tool for Investigation of Outbreaks of Gastroenteritis Caused by Campylobacter jejuni. J. Clin. Microbiol.
41: 4733-4739
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Wiesner, R. S., Hendrixson, D. R., DiRita, V. J.
(2003). Natural Transformation of Campylobacter jejuni Requires Components of a Type II Secretion System. J. Bacteriol.
185: 5408-5418
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Sails, A. D., Swaminathan, B., Fields, P. I.
(2003). Clonal Complexes of Campylobacter jejuni Identified by Multilocus Sequence Typing Correlate with Strain Associations Identified by Multilocus Enzyme Electrophoresis. J. Clin. Microbiol.
41: 4058-4067
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Tavanti, A., Gow, N. A. R., Senesi, S., Maiden, M. C. J., Odds, F. C.
(2003). Optimization and Validation of Multilocus Sequence Typing for Candida albicans. J. Clin. Microbiol.
41: 3765-3776
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Jones, N., Bohnsack, J. F., Takahashi, S., Oliver, K. A., Chan, M.-S., Kunst, F., Glaser, P., Rusniok, C., Crook, D. W. M., Harding, R. M., Bisharat, N., Spratt, B. G.
(2003). Multilocus Sequence Typing System for Group B Streptococcus. J. Clin. Microbiol.
41: 2530-2536
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Meats, E., Feil, E. J., Stringer, S., Cody, A. J., Goldstein, R., Kroll, J. S., Popovic, T., Spratt, B. G.
(2003). Characterization of Encapsulated and Noncapsulated Haemophilus influenzae and Determination of Phylogenetic Relationships by Multilocus Sequence Typing. J. Clin. Microbiol.
41: 1623-1636
[Abstract] [Full Text]
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