Division of Molecular Biology, Center for Food Safety and Applied Nutrition, Food and Drug Administration, 8301 Muirkirk Road, Laurel MD 20708, USA1
Author for correspondence: Thomas A. Cebula. Tel: +1 301 827 8281. Fax: +1 301 827 8260. e-mail: tcebula{at}cfsan.fda.gov
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ABSTRACT |
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Keywords: mutS, rpoS, horizontal gene transfer, Escherichia coli
Abbreviations: EPEC, enteropathogenic Escherichia coli; EHEC, enterohaemorrhagic Escherichia coli; SARC, Salmonella Reference Collection C; S. typhi, Salmonella enterica serovar Typhi; S. typhimurium, Salmonella enterica serovar Typhimurium
a The GenBank accession number for the sequence reported in this paper is AY050714.
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INTRODUCTION |
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Several lines of evidence demonstrate the polymorphic nature of the mutS genomic region and suggest that it has been a region active in horizontal transfer during its evolution. The mutS chromosomal region is the location for the insertion of blocks of virulence genes in the case of two widely diverged pathogens, Salmonella enterica serovar Typhimurium (S. typhimurium) and Haemophilus influenzae. In S. typhimurium, a 40 kb pathogenicity island (SPI-1) is inserted 5' to the mutS gene (Mills et al., 1995 ). In H. influenzae, a 3·1 kb tryptophanase gene cluster (tna) is inserted on the 3' side of the mutS gene in strains that cause spinal meningitis in infants. This insertion allows the utilization of tryptophan and, thus, provides a growth advantage for the pathogen, particularly in the tryptophan-rich environment of cerebro-spinal fluid. Notably, the insertion is absent from many non-pathogenic H. influenzae strains (Martin et al., 1998
).
Previously, the mutS region of the Escherichia coli chromosome was identified as having extensive genetic variability and a region that was subject to genetic exchange during the evolution of pathogenic lineages (LeClerc et al., 1999 ). A nearly identical 2·9 kb segment of DNA between the mutS and rpoS genes is found in E. coli O157:H7 and Shigella dysenteriae type 1 strains, but it is absent in E. coli K-12 and related lineages. Abutting the novel sequence in Shigella dysenteriae, an IS1 element replaces the prpB gene found in both E. coli K-12 and O157:H7, suggesting that the newly emerged O157:H7 pathogen acquired the sequence from a Shigella-like ancestor (LeClerc et al., 1999
). Recent reports have further characterized genetic polymorphisms in this region within E. coli species. An insertion of 2·1 kb, in place of the 2·9 kb insert, is found in strains of uropathogenic E. coli (Culham & Wood, 2000
), and larger intergenic regions exist in strains of enteropathogenic E. coli (EPEC) and enterohaemorrhagic E. coli (EHEC) (Herbelin et al., 2000
). In addition to the findings of genetic variability, phylogenetic analysis of EHEC and EPEC pathogens, as well as strains of the E. coli Reference (ECOR) collection, revealed that an unexpected level of recombination between mutS genes, and between surrounding sequences, has occurred during the evolution of these strains (Denamur et al., 2000
; Brown et al., 2001a
, b
). Moreover, analysis of uropathogenic E. coli strains provides further evidence for both the mosaic character of the mutSrpoS intergenic region and the horizontal transfer of mutS alleles (E. W. Brown, M. L. Kotewicz, D. J. Schu, J. Unowsky, B. Li, W. L. Payne, J. E. LeClerc and T. A. Cebula, unpublished results).
The close genetic relationship between S. typhimurium and E. coli, together with the identification of natural mutS mutators in a diverse collection of Salmonella outbreak strains, prompted us to examine the mutSrpoS region in S. typhimurium, the prototypical laboratory Salmonella strain. This study presents a comparison of the S. typhimurium mutSrpoS intergenic region to similar sequences identified in other species. Variation in the mutSrpoS region found among natural isolates of Salmonella is assessed. During the comparison of these mutSrpoS intergenic regions, the complete genome sequences of S. typhimurium (McClelland et al., 2001 ) and Salmonella enterica serovar Typhi (S. typhi) (Parkhill et al., 2001
) have been published.
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METHODS |
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Cloning.
Cosmid clones were generated from S. typhimurium, as described by Sambrook et al. (1989) . High-molecular-mass genomic DNA was isolated either by using gentle SDS and phenol/chloroform extractions or by using a PUREGENE DNA Isolation Kit (Gentra) according to the manufacturers directions. Partially digested Sau3AI genomic fragments in the 2040 kb size range were generated using a twofold enzyme dilution series. Restriction fragments were ligated into the BamHI site of cosmid pSCOS (kindly provided by S. D. Thomas and Dr G. Evans, Baylor University, Texas). After packaging the ligation mixture into bacteriophage
particles using Gigapack Gold packaging extracts (Stratagene) and infection of E. coli DH5
, kanamycin-resistant cells were selected. A library containing several thousand clones was generated.
Individual colonies of the library were grown in liquid culture in 96-well microtitre plates and spotted onto Brain Heart Infusion (BHI) agar plates containing 50 µg ampicillin ml-1. After overnight growth, the colonies were lifted onto Whatman no. 541 filter paper and processed as described previously (Kupchella et al., 1994 ). Oligonucleotide probes were labelled using T4 polynucleotide kinase and [32P]ATP (Sambrook et al., 1989
) and were used to hybridize bacterial DNA affixed to the filters. After autoradiography, positive colonies were selected from master plates. Positive colonies were purified by single-colony isolation, grown and then alkaline-lysed to prepare cosmid DNA using Midi-Maxi prep columns according to the manufacturers directions (Qiagen).
After the identification of several cosmid clones spanning the mutSrpoS region by probe and PCR analyses, cosmid cMK4 was subjected to more detailed restriction mapping, using PstI, KpnI and NotI. Four restriction fragments, encompassing the entire region between mutS and rpoS, were extracted from agarose gels and subcloned into appropriately digested pUC19 or pBluescriptKS (Stratagene) vectors. The set of subclones generated were: pBL1, a pUC19 plasmid containing a 4·2 kb KpnIKpnI fragment; pBL2, a pBluescriptKS plasmid containing a 3·5 kb KpnINotI fragment; pBL3, a pBluescriptKS plasmid containing a 3·5 NotIPstI fragment; and pBL4, a pUC19 plasmid containing a 1·8 kb PstIPstI fragment.
Long PCR.
The PCR primers used to identify and confirm positive cosmid colonies were positioned at the 3' end of mutS (5'-GTCTGGTGTAAACGTGTCAGA-3') and at the 3' end of rpoS (5'-CAATATGTGCATCGGCACAG-3'). Long PCR was performed in a Robocycler (Stratagene) using the Perkin Elmer XL Kit. The following cycling conditions were used, 94 °C for 1·5 min followed by 30 cycles at 94 °C for 1·0 min, 55 °C for 1·5 min and 68 °C for 4·5 min. As expected, cosmid clones contained approximately 35 kb of insert DNA.
Sequencing.
Plasmid inserts in pBL1 and pBL2 were sequenced commercially (Lark Technologies). The pBL3 and pBL4 inserts were sequenced in our laboratory by primer-walking sequencing of plasmid DNA and by sequencing Sau3A1 subclones. An additional sequence determination was made on pBL3 and pBL4 plasmid DNA (Amplicon Express).
Sequence analysis.
GenBank entries used for sequence comparisons included: U29579, E. coli K-12 strain MG1665 mutSrpoS intergenic region; HIU32753, H. influenzae nlpD and mutS; HIU32781 and HIU32782, H. influenzae ORFs 17; AF054420, E. coli O157:H7 mutSrpoS intergenic region; AE008832 and AE008833, S. typhimurium LT2 sections 140 and 141 of 224 of the complete genome; AL627276, S. typhi strain CT18 complete chromosome segment 12/20; Y13230, Enterobacter cloacae rpoS; AJ422108, Enterobacter cloacae rpoS, slyA, pad1 and yclC; AJ422107, Kluyvera cryocrescens rpoS (partial), slyA, pad1 and yclC (partial); Z99105, Bacillus subtilis genome segment 2 of 21. GenBank accession no. AF242211 contains the partial sequence for the mutSrpoS intergenic region of E. coli E2348/69, an EPEC 1 strain, and is representative of the EPEC 1, EPEC 2 and EHEC 2 groups of enteric pathogens. We refer to them as EPEC/EHEC strains and distinguish them from the EHEC 1 group, which includes E. coli O157:H7 (Herbelin et al., 2000 ). DNA sequence analysis was performed using the Wisconsin Package (version 10.2) of the Genetics Computer Group (GCG). BLAST and Clusters of Orthologous Groups of proteins (COG) analyses were performed at the National Center for Biotechnology (http://www.ncbi.nlm.nih.gov).
PCR and hybridization analyses of SARC strains.
Based on the S. typhimurium sequence (AY050714), oligonucleotides were synthesized to generate PCR products from specific 24 kb targets within the mutSrpoS intergenic region: S segment (2·0 kb), 5'-CGATAAGCAACCTCAAGCGAC-3' and 5'-AACGGCATAAATGCCCTGAC-3'; HK segment ORFs 12 (2·2 kb of the segment not present in E. coli K-12), 5'-TGACATCAGAGACACCCATC-3' and 5'-CGCCTTATTAAACTCATCGC-3'; HK segment ORFs 37 (4·2 kb of the segment common to E. coli K-12 and H. influenzae), 5'-AGTTGATCTCGCCATCATCC-3' and 5'-ACCGTGACTTTATCTTCTGCC-3'; O segment (2·1 kb), 5'-GTTTTCTCGTTTTACCAGCC-3' and 5'-TCACCATCTTCACATATCCC-3'. The PCR oligonucleotide primers used for sizing the HK ORFs 5/6 deletion were ORF5for (5'-TCCAGGTGCCGCTCATTGAGC-3') and ORF6rev (5'-GCCAGCAACGTTTATCGCATC-3'). The PCR conditions used were 94 °C for 1·5 min followed by 30 cycles at 94 °C for 1·0 min, 55 °C for 1·5 min and 68 °C for 1·5 min.
Probes were made by random priming of PCR products using [-32P]dATP (NEB BLOT Kit). Probe hybridization and wash conditions were as described above for oligonucleotide probes, except that strains were grown on BHI plates without the antibiotic; hybridization and washing took place at 60 °C using 6xSSC (saline sodium citrate).
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RESULTS |
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Fragments of approximately 35 kb in size were generated by partial Sau3A1 digestion of chromosomal DNA from S. typhimurium, and these were cloned into cosmid vector pSCOS. Several cosmids containing mutS and rpoS were identified by colony hybridization using Salmonella-specific probes. Four subclones were generated from one cosmid, cMK4, and sequenced. The sequence data spanning mutS to rpoS were assembled and analysed (GenBank accession no. AY050714). During the course of this work, the genome sequence for S. typhimurium was completed (McClelland et al., 2001 ).
The mutSrpoS intergenic sequence data demonstrate that the mutS and rpoS genes of S. typhimurium are separated by 12·6 kb of DNA, rather than by the 6·9 kb of DNA that separates these two genes in E. coli K-12. These data, in addition to the sequences of fhlA, SPI1 and mutS (Mills et al., 1995 ), demonstrated the gene order fhlASPI-1mutSrpoS in S. typhimurium. These results show that the orientation and position of the Salmonella mutS and rpoS genes relative to the flanking genes are the same as found for E. coli K-12 (Blattner et al., 1997
). The integrity of the cosmid clone and the size of the mutSrpoS intergenic region were verified by long-PCR analysis of genomic S. typhimurium DNA (data not shown). Publication of the complete genome sequence of S. typhimurium (including corresponding GenBank accession nos AE008832 and AE008833) has confirmed our sequence and gene assignments. The complete genome data differed from our 13163 bp sequence at two bases. Furthermore, the complete genome sequence of S. typhi (GenBank accession no. AL627276) reveals a sequence and gene arrangement in the mutSrpoS region that is highly similar to that of S. typhimurium.
Multi-gene segments in the S. typhimurium mutSrpoS intergenic region
Analysis of the 12·6 kb mutSrpoS intergenic region suggested that this region was organized into three distinct segments. Each segment is composed of a group of contiguous genes or ORFs that are also found as contiguous genes in other species. For reference, the 7·0, 2·9 and 2·7 kb Salmonella segments have been designated HK, O and S, respectively, to denote their similarities to DNA sequences in H. influenzae and E. coli K-12 (HK), in E. coli O157:H7 and Shigella dysenteriae type 1 (O), and in Salmonella species (S) (Fig. 1).
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Comparisons of the Salmonella HK segment with the mutSrpoS intergenic region of E. coli K-12 revealed the presence of similar coding sequences for ORFs 37. The nucleotide similarity between these Salmonella and E. coli K-12 ORF sequences ranges from 73 to 77% (Table 1). In place of HK ORFs 1 and 2 found in Salmonella, a single ORF, o454, is found in E. coli K-12 (Fig. 1
). As depicted in Fig. 1
, the orientation of the HK segments in Salmonella and E. coli is inverted relative to the mutS and rpoS genes in the two species. In addition to the HK segments in H. influenzae, Salmonella and E. coli, analysis for Clusters of Orthologous Groups of proteins (COG) showed one other set of contiguous HK ORFs in Pasteurella multocida (GenBank accession nos AE006173 and AE006174). This segment of contiguous HK ORFs is not located near mutS on the P. multocida chromosome.
The O segment
A 2·9 kb segment of DNA adjacent to the rpoS gene of S. typhimurium is 81% similar to a 2·9 kb sequence in the mutSrpoS intergenic region of pathogenic E. coli O157:H7. The sequence was identified as a novel sequence in E. coli O157:H7 because of its absence in E. coli K-12 (LeClerc et al., 1996 ). A sequence identical to that in E. coli O157:H7 abuts an IS1 insertion element in Shigella dysenteriae type I strains (LeClerc et al., 1999
). As is the case for the HK segment, the O segment lies in inverted orientations in the Salmonella and E. coli lineages (Fig. 2
).
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The S segment
A 2·7 kb sequence that abuts the end of mutS in S. typhimurium (Fig. 1) was designated as the S segment because it was characteristic for Salmonella species and was absent in E. coli strains. No similar sequence is present in the complete genomes of E. coli K-12 or E. coli O157:H7, nor in the other E. coli sequences in GenBank. The same position in E. coli strains is occupied by o218 (Fig. 1
), which encodes a protein phosphatase (prpB, Missiakas & Raina, 1997
; also designated pphB, Blattner et al., 1997
); o218 has no sequence similarity to ORFs found in the S segment.
The 2·7 kb S segment of S. typhimurium shows 65% nucleotide similarity to 2·7 kb of DNA found between the slyA and rpoS genes of a clinical isolate of Enterobacter cloacae (GenBank accession no. AJ422108). The O segment in E. cloacae is inverted relative to its orientation in S. typhimurium (Fig. 2). The same arrangement and orientation of the S and O segments found in E. cloacae, relative to the mutS and rpoS genes, is seen in Klebsiella pneumoniae (Washington University Genome Sequencing Center; http://genome.wustl.edu/gsc). Upon the examination of additional genome sequence data, Clusters of Orthologous Groups of proteins (COG) analysis showed that the S segment ORFs are found in Pseudomonas aeruginosa (GenBank accession no. AE004560). In P. aeruginosa, the contiguous S segment ORFs are not located near the mutS and rpoS genes on the chromosome.
Segments in strains of the SARC collection
To examine the presence of the S, HK and O segments across a broad spectrum of Salmonella strains, colony hybridization using PCR probes generated from each of the segments in S. typhimurium was performed on strains from the SARC collection. The SARC collection contains two representative strains from each of eight characterized Salmonella groups, chosen to be broadly representative of the genetic diversity within Salmonella species (Boyd et al., 1996 ). Random primer labelling of PCR probes spanning 24 kb and non-stringent hybridization conditions were used to assure the recognition of target sequences. Two probes were used for the analysis of the HK segment, since it comprises sequence similar to H. influenzae (ORFs 17) and E. coli K-12 (ORFs 37). In Table 2
the probe designated H hybridizes to ORFs 1 and 2, and the probe designated K hybridizes to ORFs 37.
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Three strains did not show the patterns expected for hybridization to the S, HK and O segments (Table 2). The S segment probe did not hybridize with SARC3, a SARC group II strain, and the H probe for ORFs 1 and 2 failed to hybridize with SARC5 and SARC6, both Salmonella arizonae strains of SARC group IIIA.
Long-PCR analysis was performed on chromosomal DNA from each of the 16 SARC strains, to further characterize their mutSrpoS intergenic regions. Using PCR primers from sites within the conserved mutS and rpoS genes, a 13·8 kb PCR product characteristic of S. typhimurium was produced in 12 of these strains (Fig. 3). SARC5 and SARC6, the two S. arizonae strains of group IIIa, yielded 8·5 kb products, which indicated a deletion of about 5 kb relative to the 13·8 kb PCR product. This result is consistent with the lack of hybridization of the H probe in these strains. The SARC3 strain showed a PCR product of 11·7 kb, indicating a deletion of about 2 kb, consistent with the probing data, which showed the lack of hybridization within the S segment.
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DISCUSSION |
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In the HK segment, the ordered contiguous ORFs 17 relate DNA sequences across species as broadly divergent as Salmonella and H. influenzae, and they thus reiterate the chromosomal linkage within their last common ancestor (de Rosa & Labedan, 1998 ). Similar initiation and termination codon positions for the seven HK ORFs in S. typhimurium and H. influenzae reinforce this relationship. Furthermore, three pairs of ORFs in the HK segment show overlapping initiation and termination codons, such as within the sequence ATGA. This overlap, or translational coupling, has been shown to link the expression of genes whose co-expression or protein product ratios are critical (Andre et al., 2000
). In the complete genome sequence of E. coli K-12, 9% of ORFs show translational coupling (Blattner et al., 1997
). In the HK segment of S. typhimurium, translational coupling occurs at the sequence ATGA for ORF pair 1 and 2 and for ORF pair 4 and 5; ORF pair 5 and 6 is also translationally coupled within an ATGTTAA sequence. In H. influenzae, ORFs 4 and 5 are translationally coupled within an ATGA sequence. In the O segment in S. typhimurium, o120 and o402 are translationally coupled within the sequence ATGA. The long-term retention of contiguous ORFs and these translational overlaps suggest functional linkages within the HK segment, as in the retention of functionally related members of operons.
Evolution of mutSrpoS intergenic regions: chromosomal inversions and segment insertions and deletions
Sequences with similarity to each of the three segments (HK, O and S) present in the mutSrpoS intergenic region from S. typhimurium were found in an inverted orientation in E. coli K-12, E. coli O157:H7 or Enterobacter cloacae strains (Fig. 2). The nucleotide and amino-acid similarities, as well as the conservation of ORFs, among the HK, O and S segments of Salmonella and Escherichia coli strains might be anticipated from the overall similarities between the genomes of these organisms, yet finding multiple inverted short segments within a limited region (10 kb) of the chromosome was unexpected.
Some inversions within chromosomes, characteristically centred about the axis of replication, seem to reflect ancient changes within bacteria [see reviews by Hughes (2000) and Eisen et al. (2000)
]. Previous comparisons of the Salmonella and E. coli genetic maps demonstrated a large inversion with end points near map positions 26 and 36 min (Smith et al., 1990
; Sanderson et al., 1996
). Naturally occurring large inversions have been noted in the chromosome of S. typhi, where the chromosome appears to have been shuffled by recombination between homologous rRNA genes (Liu & Sanderson, 1996
, 1998
). Recently, three large inversions have been characterized for Salmonella enterica serovar Pullorum, a fowl-adapted pathogen (Liu et al., 2002
). In comparison to the above large chromosomal inversions, the inversions of short segments located between the mutS and rpoS genes in the Salmonella and E. coli genomes represent a new type of polymorphism between closely related bacterial species.
There is a contrast between the orderly accumulation of point mutations and the punctuated changes caused by such inversions or the insertion or deletion of segments in a chromosome. We have attempted to understand the evolution of the mutSrpoS intergenic region, including segment orientations and the insertion or deletion of segments, by comparing the sequences of closely related strains/species. It is useful to examine the structural changes that have taken place in this chromosomal region in the context of enterobacterial evolution. The phylogenetic history of the enteric species has been constructed from highly conserved 16S rRNA sequences (see Dauga, 2002 ). Of note is the observation that Klebsiella and Enterobacter appear to have diverged earlier in enterobacterial evolution (i.e. they are more ancestral in the family tree), while Salmonella and E. coli emerged later. Klebsiella and Enterobacter both have a mutSrpoS intergenic region containing the S and O segments (Fig. 2
), suggesting that the ancestral enterobacterial genome also contained these two segments. The addition of the HK segment and the inverted orientations of segments between Salmonella and Escherichia coli suggest that these changes occurred later in the evolution of enteric bacteria and represent more recently acquired configurations in the mutSrpoS intergenic regions of Salmonella and E. coli species.
Elements of the large intergenic region of Salmonella are most similar to those found in EPEC and EHEC strains (Herbelin et al., 2000 , and Fig. 2
). These pathogenic E. coli strains contain homologues of both the Salmonella HK segment and the O segment. The simplest model to account for these strain differences is that two inversions, one of the HK segment and another of the O segment, have occurred since Salmonella and E. coli shared a common ancestor that contained the large intergenic region (Herbelin et al., 2000
).
Simple inversions, however, fail to explain the different ORFs found at inversion junctions in Salmonella and E. coli. In one example, ORFs 1 and 2 in the HK segment in Salmonella are absent in known E. coli strains. Salmonella ORFs 1 and 2 are replaced by o454 in E. coli strains. Although superficially resembling ORF 1 in its position and size, o454 shows only 46% nucleotide similarity with ORF 1, compared to similarities of 7377% with ORFs 37 (Table 1). Furthermore, the amino-acid similarity between E. coli o454 and Salmonella ORF 1 is 49%, far lower than the mean 85% similarity exhibited by the other HK cohorts (Table 1
). Protein BLAST analysis indicates that both ORF 1 and o454 belong to the permease families of transporters with strong similarity to gluconate-transport proteins. The nucleotide and amino-acid comparisons, however, as well as the absence of the contiguous ORF 2 in E. coli, argue that o454 of E. coli and ORF 1 of Salmonella are not homologues and that o454 has been substituted for Salmonella ORFs 1 and 2.
In another example, o218 (protein phosphatase prpB) is found next to the 3' end of mutS in E. coli at the junction of the inverted versions of the HK segment. The S segment occurs at this position in Salmonella. The absence of o218 next to mutS in Salmonella, and in the evolutionarily older genus Klebsiella, suggests that its acquisition in the E. coli lineage was more recent. This contradicts the hypothesis that o218 is present in the common ancestor of both Salmonella and E. coli (Herbelin et al., 2000 ). Salmonella species do contain o216, which is 61% similar to o218 (see Fig. 2
). o216 has been referenced as pigE (pathogenicity island gene, Pancetti & Galan, 2001
) and as pphB (protein phosphatase, McClelland et al., 2001
; also see Shi et al., 2001
). o216 is found on the 5' side of mutS next to or as part of the SPI pathogenicity island insertion in Salmonella, whereas o218 is found on the 3' side of mutS in the E. coli lineage. We, therefore, propose that o216 and o218 have been independently acquired by the Salmonella and E. coli lineages, respectively.
The large and probably ancestral-like mutSrpoS intergenic region in S. typhimurium, containing the HK, O and S segments identified here, is present in much of the genetic spectrum of Salmonella as represented by the SARC collection of 16 strains. The exceptions to this are the apparent absence of HK ORFs 1 and 2 in SARC group IIIA, the loss of the S segment in SARC3 and the deletion at the ORF 5/6 junction in SARC2 and other S. typhi strains. These changes are likely to represent recombinational shuffling in the mutSrpoS region, whose polymorphic character is more apparent among E. coli strains when similar comparisons are made. Two points may be made here. First, recombination in the region may lead to more subtle changes, such as intragenic recombinations, which will be best uncovered by sequence analysis. In this light, the examination of mutS sequence evolution among SARC strains has implicated a role for intragenic recombination in the S. typhi SARC2 strain mentioned above, at a site within the mutS gene upstream of the characterized deletion (Brown et al., 2002 ). Second, comparisons of Salmonella strains within a group i.e. strains that share a pathological niche may show exchange on a greater scale than the broadly representative strains of the SARC collection. The surprisingly high incidence (>1%) of mutS mutators among natural isolates of Salmonella (LeClerc et al., 1996
; LeClerc & Cebula, 2000
) and the heightened ability of these mutators to recombine foreign DNA with host sequences (Matic et al., 1995
) make such exchanges likely.
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SUMMARY |
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ACKNOWLEDGEMENTS |
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Received 8 January 2002;
revised 14 May 2002;
accepted 14 May 2002.