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Pathogenicity and Medical Microbiology |
INSERM U4581, Laboratoire d’études de génétique bactérienne dans les infections de l’enfant (EA3105)2, Hôpital Robert Debré, 48 Boulevard Sérurier 75019 Paris, France
Département d’Anthropologie Génétique, Bordeaux II, 3 Place de la Victoire, 33000 Bordeaux, France3
Laboratoire de Microbiologie, Faculté de médecine de Brest, 22 Avenue Camille Desmoulins, B.P. 815, 29285 Brest Cedex, France4
Author for correspondence: Erick Denamur. Tel: +33 1 400 31916. Fax: +33 1 400 31903. e-mail: denamur{at}infobiogen.fr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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Keywords: Escherichia coli, phylogeny, commensal, virulence
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). Commensal enteric E. coli may therefore be the natural reservoir of pathogenic strains (Falkow, 1996 ). Intestinal or extraintestinal E. coli infections are caused by strains harbouring numerous virulence factors located on plasmids, bacteriophages, or the bacterial chromosome (Mühldorfer & Hacker, 1994 ). Several studies have shown that pathogenic E. coli strains may be derived from commensal strains by the acquisition of chromosomal or extra-chromosomal virulence operons (Finlay & Falkow, 1997 ; Ochman et al., 2000 ). ‘Black hole’ genomic deletions that enhance pathogenicity (Maurelli et al., 1998 ) or random functional point mutations that are adaptive for pathogenic environments (Sokurenko et al., 1998 ) may also represent additional strategies of genome plasticity by which a commensal strain may become virulent. Many of these observations were made possible by the fact that E. coli populations have a clonal structure (Selander & Levin, 1980 ). Four main phylogenetic groups, A, B1, B2 and D, were described by Herzer et al. (1990) using multilocus enzyme electrophoresis with the 72 strains of the E. coli reference (ECOR) collection (Ochman & Selander, 1984 ). This finding was subsequently confirmed by Desjardins et al. (1995) , by comparison of several genetic markers. The assignment of E. coli clones to one of these four groups is the basis of phylogenetic studies of the species. Phylogenetic analyses have indicated several origins for diverse natural populations of pathogenic E. coli and Shigella strains (Pupo et al., 1997 ). Thus, Shigella clones are derived from E. coli outside the phylogenetic groups B2 and A (Rolland et al., 1998 ; Pupo et al., 2000 ), whereas verotoxin-producing E. coli O157:H7 clones could belong to phylogenetic group D (Clermont et al., 2000 ). The clones responsible for human extraintestinal infections frequently belong to the anciently diverged B2 phylogenetic group (Lecointre et al., 1998 ; Picard et al., 1999 ).
The population structure of several pathogenic isolates has been extensively studied but little is known about the structure of commensal strain populations. It is therefore mandatory to determine the intraspecies phylogenetic relationships of E. coli isolates from the normal gut flora of healthy humans, to establish a background database for further studies on pathogenic strains. In this study, we used a recently described method facilitating the rapid and simple determination of E. coli phylogenetic group (Clermont et al., 2000 ) in 168 non-epidemiologically related isolates from three geographically distinct human populations. This technique is based on a triplex PCR using a combination of two genes (chuA and yjaA) and an anonymous DNA fragment. The results obtained were strongly correlated with those obtained by multilocus enzyme electrophoresis and ribotyping methods (Clermont et al., 2000 ). The distributions of several known extraintestinal virulence factors (pap, afa, sfa/foc adhesin-encoding operons, hly and aer operons and ibeA and cnf1genes) were also determined.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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PCR grouping.
The phylogenetic group to which the E. coli strains belonged was determined by a PCR-based method as described previously (Clermont et al., 2000 ). Briefly, a two-step triplex PCR was performed directly on 3 µl bacterial lysate. The primer pairs used were ChuA.1 (5'-GACGAACCAACGGTCAGGAT-3')/ChuA.2 (5'-TGCCGCCAGTACCAAAGACA-3'), YjaA.1 (5'-TGAAGTGTCAGGAGACGCTG-3')/YjaA.2 (5'-ATGGAGAATGCGTTCCTCAAC-3') and TspE4C2.1 (5'-GAGTAATGTCGGGGCATTCA-3')/TspE4C2.2 (5'-CGCGCCAACAAAGTATTACG-3'). The PCR steps were as follows: denaturation for 4 min at 94 °C, 30 cycles of 5 s at 94 °C and 10 s at 59 °C, and a final extension step of 5 min at 72 °C. The data of the three amplifications resulted in assignment of the strains to phylogenetic groups as follows: chuA+, yjaA+, group B2; chuA+, yjaA-, group D; chuA-, TspE4.C2+, groupB1; chuA-, TspE4.C2-, group A (Clermont et al., 2000 ).
Detection of virulence factors.
Virulence factors were detected by amplifying the corresponding gene (ibeA, pap, afa, sfa/foc, hly, cnf1 and aer) from DNA by PCR as described previously (Picard et al., 1999 , 2001 ).
Statistical analysis.
In addition to the data obtained experimentally in this work, the commensal strains were compared with two previously analysed collections of extraintestinal pathogenic strains (Bingen et al., 1998 ; Picard et al., 1999 ). The frequencies of various phylogenetic groups in the human populations were compared using the 
2 test and the distributions of the number of virulence factors were compared using the Mann–Whitney U-test. All these tests were carried out using the Statview 4.5 software (Abacus Concept). A P value less than 0·05 was considered to show a significant difference.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). The rarity of B2 group strains confirms previous findings obtained with carboxylesterase B electrophoretic typing, which indicated that the carboxylesterase B2 type [which corresponds to phylogenetic group B2 (Picard et al., 1987 )] accounts for 9% of commensal human isolates and 1·6% of animal isolates (Goullet & Picard, 1986a ).
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2 test) increasing gradient of A group strains from Malian to French via Croatian populations (24–61%) which correlates with a significant (2 test) decreasing gradient of B1 group strains (58–12·5%). Thus, a predominance of A strains in the French population and of B1 strains in the Malian population was observed. Our data also show that the proportion of B2 phylogenetic group strains differs between populations. These strains are found in Malian populations at a frequency similar to that in animals (2%), whereas they account for almost one-fifth of the Croatian commensal E. coli. (Table 1
). A previous study of E. coli commensal strains from animals and humans originating mainly from France and Africa, based on the electrophoretic polymorphism of esterases, showed a clear delineation between (i) French human commensal isolates and (ii) African human and animal isolates (Picard et al., 1990 ). These differences in the distribution of the phylogenetic groups among the commensal strains of geographically different populations may be due to three main factors: (i) geographic/climatic conditions, (ii) dietary factors and/or the use of antibiotics, or (iii) host genetic factors; some E. coli strains may be primarily adapted to the gut conditions of certain populations. Analysis of the genetic structure of natural populations of E. coli in wild hosts on different continents suggest that strains are organized into an ecotypic structure in which adaptation to the host plays an important role in the population structure (Souza et al., 1999 ).
Distribution of extraintestinal virulence genes among human commensal strains
Extraintestinal virulence genes were rarely detected among human commensal strains, as none of the seven virulence genes studied was detected in 74·4% of strains. Only 11·3, 1·2 and 3·6% of strains contained the pap, afa and sfa/foc adhesin-coding operons, respectively. The aer determinant was found in 16% of strains whereas the remaining virulence determinants were detected in less than 5% of strains (Table 2). These proportions differed according to the phylogenetic origin of the strains. The strains most frequently bearing virulence factors were those belonging to phylogenetic group B2, in which two or three virulence genes were often detected per strain (Table 3). The 43 strains harbouring at least one virulence gene (25·6% of the 168 strains) included 28 harbouring one, 9 harbouring two, 2 harbouring three, 2 harbouring four and 2 harbouring five virulence genes (Table 3). The strains from Mali harboured fewer virulence factors than did the Croatian (U-test, P=0·005) and French (U-test, P=0·0039) isolates, as only one Malian strain (B2 group) possessed two virulence factors versus 23 strains in Croatia and 19 strains in France.
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; Hagberg et al., 1981 ; Goullet & Picard, 1986b ; Opal et al., 1990 ; Siitonen, 1992 ; Hilali et al., 2000 ). The frequent occurrence of commensal strains with virulence determinants reported by Mühldorfer et al. (1996) may be due to a local epidemiological bias, as no such prevalence was found by these workers in Peru (Hacker et al., 1983 ).
Comparison of human commensal strain data with data obtained from two extraintestinal pathogen collections
The phylogenetic grouping of strains used for comparison were all obtained by the PCR triplex method. The 69 neonatal meningitis strains (Bingen et al., 1998 ) and the 49 strains isolated from miscellaneous extraintestinal infections in adults (Picard et al., 1999 ) were reanalysed by the PCR grouping method and the results obtained were strongly correlated with those of ribotyping (Clermont et al., 2000 and data not shown). Virulence determinants were also detected using the same approach. The cnf1 data for the pathogen collections are unpublished.
Of the 118 extraintestinal pathogenic strains, 110 (93%) harboured at least one virulence gene. The human commensal strains had fewer virulence factors than the extraintestinal pathogenic strains (U-test, P<0·0001). This was also true for the frequencies of each individual virulence determinant, except for afa, which was under-represented (Table 2).
Pathogenic strains were distributed among phylogenetic groups as follows: A, 11 strains (9%); B1, 3 strains (2·5%); D, 19 strains (16%) and B2, 85 strains (72%). If virulence determinant frequencies were compared by phylogenetic group between the commensal and extraintestinal pathogenic series, the commensal strains of phylogenetic groups A, B1 and D appeared to possess fewer virulence determinants (U-test, P<0·0001,=0·0017 and <0·0001, respectively). In contrast, no significant difference was observed between the phylogenetic B2 strains. This absence of difference was also found for each virulence gene (Table 3).
In addition, confirming that the strains of phylogenetic group B2 are more frequent among extraintestinal pathogenic strains (40–72%) than among commensal strains (9–11%) (Goullet & Picard, 1986b ; Johnson et al., 1991 ; Bingen et al., 1998 ; Picard et al., 1999 ; Hilali et al., 2000 ; this work), our homogeneous dataset also increases our understanding of the emergence of virulence in human extraintestinal infections. The smaller number of virulence determinants in commensal strains of phylogenetic groups A, B1 and D than in the corresponding pathogenic strains is consistent with the hypothesis (Bingen et al., 1998 ; Lecointre et al., 1998 ; Picard et al., 1999 ) that these strains acquire virulence factors by horizontal transfer, enabling them to become virulent and to invade immunocompetent hosts (Picard & Goullet, 1988 ) from the host’s intestinal reservoir. In contrast, the strains of phylogenetic group B2 in the commensal flora appear to be potentially virulent. This intrinsic virulence may explain why strains of phylogenetic group B2 are frequently isolated from patients with extraintestinal infections, despite their rarity in the gut flora.
Concluding remarks
This work on a relatively small number of commensal strains clearly demonstrates that the commensal flora has a complex population structure, which depends on ecotype. As commensal enteric isolates are believed to be the reservoirs of pathogenic strains, it will be interesting to determine whether the geographic differences between E. coli commensal populations are associated with differences in the distribution of diseases caused by different types of E. coli. Studies on a large number of commensal strains including precise geographic, socio-economic and medical data are needed to provide further insight into the emergence of virulent E. coli clones.
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ACKNOWLEDGEMENTS |
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Received 25 October 2000;
revised 1 February 2001;
accepted 14 February 2001.
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