supplementary material (includes 3 tables numbered table ...€¦ · web viewsupplementary...

Supplementary Material (includes 3 tables numbered table S1 to S3)

Supplementary Material (includes 3 tables numbered table S1 to S3)

Table S1.

Collection of strains used in the study with their origins.

Strain ID

Source

JM221

Mathewson et al. 1987

17-2

Nataro et al. 1993

255/1-1

JP Girardeau-INRA

H10407

Evans et al. 1975

DAEC395

Forestier et al. 1996

DAECT2

Scaletsky et al. 2002

DAEC483


DAEC7


E2539-C1

Tornieporth et al. 1995

EDL1493


ECOR10

Ochman and Selander 1984

ECOR20


ECOR13


ECOR1


DEC6a

Reid et al. 1999

ECOR24


ECOR17


ECOR4


EIEC85b

Escobar-Páramo et al. 2003

ECOR23


DAEC5


DEC9a

Reid et al. 1999

DEC8b

Reid et al. 1999

55989

Bernier et al. 2002

248/1-2

JP Girardeau-INRA

DEC11a

Reid et al. 1999

DEC12a

Reid et al. 1999

DEC13a

Reid et al. 1999

ECOR68


H-19

Smith et al. 1983

DEC10a

Reid et al. 1999

469

Yves Germani-Inst.Pasteur

TX-1


ECOR26


ECOR27


11097

Bernier et al. 2002

ECOR45


384P

Bernier et al. 2002

DAEC221


DEC15a

Reid et al. 1999

DAECT437


ECOR58


ECOR34


11074

Bernier et al. 2002

440

Yves Germani-Inst.Pasteur

DEC14a

Reid et al. 1999

DAEC126


DAECT179


ECOR70


DEC7a

Reid et al. 1999

SB01-97


SS92a


SB11-56


SD01-77


EDL933

Perna et al. 2001

RIMD0509952

Hayashi et al. 2001

ECOR37


EDL931

Bohm et al. 1992

DEC5d

Reid et al. 1999

DEC3a

Reid et al. 1999

DEC4a

Reid et al. 1999

DAEC218


ECOR50


ECOR49


DAEC19


56390

Bernier et al. 2002

DAECT192


ECOR47


ECOR46


DAEC141


DAEC162


ECOR35


DAEC9


ECOR40


ECOR41


DAECT14


042

Nataro et al. 1985

DAECT19


ECOR60


ECOR59


2348/69

Levine et al. 1978

DEC1a

Reid et al. 1999

DEC2a

Reid et al. 1999

ECOR51


ECOR52


CFT073

Welch et al. 2002

ECOR57


ECOR62


RS218

Silver et al. 1980

ECOR64


DAEC18


EC7372

Pham et al. 1997

DAEC11


IH11128

Vaisanen-Rhen 1984

DAEC20


C1845

Bilge et al. 1989

381A

Bernier et al. 2002

DAEC213


E. fergusonii

Lawrence et al. 1991

Literature cited

Bernier, C., P. Gounon, and C. Le Bouguénec. 2002. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect. Immun. 70:4302-4311.

Bilge, S. S., C. R. Clausen, W. LAu, and S. L. Moseley. 1989. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J. Bacteriol. 17:4281-4289.

Bohm, H., and H. Karch. 1992. DNA fingerprinting of Escherichia coli O157:H7 strains by pulsed-field gel electrophoresis. J. Clin. Microbiol. 30:2169-2172.

Escobar-Páramo, P., C. Giudicelli, C. Parsot, and E. Denamur. 2003. The evolutionary history of Shigella and enteroinvasive Escherichia coli revised. J. Mol. Evol. 57:140-148.

Evans, D. G., R. P. Silver, D. J. Evans, D. G. Chase, and S. L. Gorbach. 1975. Plasmid-controlled colonization factor associated with virulence in Escherichia coli enterotoxigenic for humans. Infect. Immun. 12:656-667.

Forestier, C., M. Meyer, S. Favre-Bonte, C. Rich, G. Malpuech, C. Le Bouguénec, J. Sirot, B. Joly, and C. De Champs. 1996. Enteroadherent Escherichia coli and diarrhea in children: a prospective case-control study. J. Clin. Microbiol. 34 :2897-2903.

Hayashi, T., K. Makino, M. Ohnishi, K. Kurokawa, K. Ishii, K. Yokoyama, C.-G. Han, E. Ohtsubo, K. Nakayama, T. Murata, M. Tanaka, T. Tobe, T. Iida, H. Takami, T. Honda, C. Sasakawa, N. Ogasawara, S. Yasunaga, T. Shiba, M. Hattori, and H. Shinagawa. 2001. Complete genome sequence of enterohemorragic Escherichia coli O157:H7 and genomic comparison with laboratory strain K-12. DNA Res. 8:11-22.

Lawrence, J. G., H. Ochman, and D. L. Hartl. 1991. Molecular and evolutionary relationships among enteric bacteria. J. Gen. Microbiol. 137:1911-1921.

Levine, M. M., E. J. Bergquist, D. R. Nalin, D. H. Waterman, R. B. Hornick, C. R. Young, S. Stoman, and B. Rowe. 1978. Escherichia coli strains that cause diarrhea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet I:119-122.

Mathewson, J. J., R. A. Oberhelman, H. L. Dupont, F. Javier de la Cabada , and E. V. Garibay. 1987. Enteroadherent Escherichia coli as a cause of diarrhea among children in Mexico. J Clin Microbiol. 25:1917-9.

Nataro, J. P., M. M. Baldini, J. B. Kaper, R. E. Black, N. Bravo, and M. M. Levine. 1985. Detection of an adherence factor of enteropathogenic Escherichia coli with DNA probe. J. Infect. Dis. 152:560-563.

Nataro, J. P., D. Yikang, J. A. Giron, S. J. Savarino, M. H. Kothary, and R. Hall. 1993. Aggregative adherence fimbria I expression in enteroaggregative Escherichia coli requires two unlinked plasmid regions. Infect. Immun. 6:1126-1131.

Ochman, H., and R. K. Selander. 1984. Standard reference strains of Escherichia coli from natural populations. J. Bacteriol. 157:690-692.

Perna, N. T., G. Plunkett III, V. Burland, B. Mau, J. D. Glasner, D. J. Rose, G. F. Mayhew, P. S. Evans, J. Gregor, H. A. Kirkpatrick, G. Posfais, J. Hacket, S. Klink, A. Boutin, Y. Shao, L. Miller, E. J. Grotbeck, N. W. Davis, A. Lim, E. T. Dimalanta, K. D. Potamousis, J. Apodaca, T. S. Anantharaman, J. Lin, G. Yen, D. C. Schwartz, R. A. Welch, and F. R. Blatner. 2001. Genome sequence of enterohemorrhagic Escherichia coli O157:H7. Nature 409:529-533.

Pham, T. Q., P. Goluszko, V. Popov, S. Nowicki, and B. J. Nowicki. 1997. Molecular cloning and characterization of Dr-II, a nonfimbrial adhesin-I-like adhesin isolated from gestational pyelonephritis-associated Escherichia coli that binds to decay-accelerating factor. Infect. Immun. 65:4309-4318.

Reid, S. D., C. J. Herbelin, A. C. Bumbaugh, R. K. Selander, and T. S. Whittam. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:64-67.

Scaletsky, I. C., S. H. Fabbricotti, R. L. Carvalho, C. R. Nunes, H. S. Maranhao, M. B. Morais, and U. Fagundes-Neto. 2002. Diffusely adherent Escherichia coli as a cause of acute diarrhea in young children in Northeast Brazil: a case-control study. J. Clin. Microbiol. 40:645-648.

Silver, R. P., W. Aaronson, A. Sutton, and R. Schneerson. 1980. Comparative analysis of plasmids and some metabolic characteristics of Escherichia coli K1 from diseased and healthy individuals. Infect. Immun. 29:200-206.

Smith, H. W., P. Green, and Z. Parsell. 1983. Vero cell toxins in Escherichia coli and related bacteris:transfer by phage and conjugation and toxic action in laboratory animals, chicken and pigs. J. Gen. Microbiol. 129:3121-3137.

Tornieporth, N. G., J. John, K. Salgado, P. de Jesus, E. Latham, M. C. Melo, S. T. Gunzburg, and L. W. Riley. 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J. Clin. Microbiol. 33:1371-1374.

Vaisanen-Rhen, V. 1984. Fimbria-like hemagglutinin of Escherichia coli O75 strains. Infect. Immun. 46:401-407.

Welch, R. A., V. Burland, G. Plunkett III, P. Redford, P. Roesch, D. Rasko, E. L. Buclkes, S.-R. Liou, A. Boutin, J. Hackett, D. Stroud, G. F. Mayhew, D. J. Rose, S. Zhou, D. C. Schwartz, N. T. Perna, H. L. T. Mobley, M. S. Donnenberg, and F. R. Blatner. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 99:17020-17024.

Table S2

List of the primers used for the sequencing of the six essential genes (trpA to polB) used in the strain phylogenetic analysis as well as those used to generate the specific probes for detecting the presence of the different VFs and to perform their sequences.

Gene

Primer sequence

Source

trpA

5’-ATGGAACGCTACGAATCTCTGTTTGCCC-3’


5’-TCGCCGCTTTCATCGGTTGTACAAA-3’

trpB

5’-ACAATGACAACATTACTTAACCCCT-3’


5’-TTTCCCCTCGTGCTTTCAAAATATC-3’

pabB

5’-TTTTACACTCCGGCTATGCCGATCA-3’

Guttman and Dykhuizen 1994

5’-GCTGCGGTTCCAGTTCGTCGATAAT-3’

putP

5’-GCGACGATCCTTTACACCTTTATTG-3’


5’-CGCATCGGCCTCGGCAAAGCG-3’

icd

5’-GAAAGTAAAGTAGTTGTTCCGG-3’

Escobar-Páramo et al. in press

5’-GATGATCGCGTCACCAAAYTC-3’

polB

5’-TCAACGCCTGGTTTGCCAACTA-3’

Bjedov et al. 2003

5’-TCCAGTTCTAATGCGCTGGTCA-3’

papC

5’-GACGGCTGTACTGCAGGGTGTGGCG-3’

Le Bouguenec et al., 1992

5’-ATATCCTTTCTGCAGGGATGCAATA-3’

papG

5’-GGGATGAGCGGGCCTTTGAT-3’

Johnson and Brown 1996

5’-CGGGCCCCCAAGTAACTCG-3’

5’-GGCCTGCAATGGATTTACCTGG-3’

5’-CCACCAAATGACCATGCCAGAC-3’

sfa/foc

5’-CTCCGGAGAACTGGGTGCATCTTAC-3’


5’-CGGAGGAGTAATTACAAACCTGGCA-3’

sfaS

5’-GTGGATACGACGATTACTGTG-3’

Johnson and Stell 2000

5’-CCGCCAGCATTCCCTGTATTC-3’

focG

5’-CAGCACAGGCAGTGGATACGA-3’

Johnson and Stell 2000

5’-GAATGTCGCCTGCCCATTGCT-3’

iroN

5’-AATCTTACCGGCAATAGCGC-3’

Bonacorsi et al. 2003

5’-GCTATAACGCACGGAGTTAC -3’

hlyCA

5’-AGGTTCTTGGGCATGTATCCT-3’

Bingen et al. 1998

5’-TTGCTTTGCAGACTGCAGTGT-3’

cnf1

5’-CAGTGACCGGATCTCCGTTAT-3’

Picard et al. 2001

5’-CGTGTAATTCTTCTGTACTTCC-3’

hra

5’-CAGAAAACAACCGGTATCAG-3‘

Bingen-Bidois et al. 2002

5’-ACCAAGCATGATGTCATGAC-3’

chuA

5’-GACGAACCAACGGTCAGGAT-3’

Clermont et al. 2000

5’-TGCCGCCAGTACCAAAGACA-3’

iucC

5'-AAACCTGGTTTACGCAACTGT-3'

Bingen et al. 1998

5’-ACCCGTCTGCAAATCATGGAT-3’

afaBC/daaC

5’-GCTGGGCAGCAAACTGATAACTCTC-3’


5’-CATCAAGCTGTTTGTTCGTCCGCCG-3’

afaD

5’-GAAAGCGGTAAGCTGAAGGC-3’

This study

5’-CCGGTGAAATAAATACTCTC-3’

M030

5'-GATCAGCGCCACAATTAC-3'

Blanc-Potard et al. 2002

5'-CAGTGGAGTCTGCTGCTC-3'

AA

5’-CTGGCGAAAGACTGTATCAT-3’

Baudry et al. 1990

5’-CAATGTATAGAAATCCGCTGTT-3’

eaeA

5’-GCAAATTTAGGTGCGGGTCAGCGTT-3’

Germani et al. 1997

5’-GGCTCAATTTGCTGAGACCACGGTT-3’

bfpA

5’-CAATGGTGCTTGCGCTTGCT-3’


5’-GCCGCTTTATCCAACCTGGT-3’

ST

5’-TCTGTATTGTCTTTTTCACC-3’


5’-TTAATAGCACCCGGTACAAGC-3’

LT

5’-GCGACAAATTATACCGTGCT-3’


5’-CCGAATTCTGTTATATATGT-3’

stx1

5’-GAAGAGTCCGTGGGATTACG-3’

Pollard et al. 1990

5’-AGCGATGCAGCTATTAATAA-3’

stx2

5’-TTAACCACACCCACGGCAGT-3’

Pollard et al. 1990

5’-GCTCTGGATGCATCTCTGGT-3’

ehxA

5’-ACGATGTGGTTTATTCTGGA-3’

Schmidt et al. 1995

5’-CTTCACGTCACCATACATAT-3’

ipaB

5’-GGACGCAATTCAGGATATCAAGGAG-3’


5’-GCCCCAAGTATTTTCCCAACACAAC-3’

Literature cited

Baudry, B., S. J. Savarino, P. Vial, J. B. Kaper, and M. M. Levine. 1990. A sensitive and specific DNA probe to identify enteroaggregative Escherichia coli, a recently discovered diarrheal pathogen. J. Infect. Dis. 161:1249-1251.

Bjedov, I., G. Lecointre, O. Tenaillon, C. Vaury, M. Radman, F. Taddei, E. Denamur, and I. Matic. 2003. Polymorphism of gene encoding SOS polymerases in natural populations of Escherichia coli. DNA Repair 2:417-426.

Bingen, E., B. Picard, N. Brahimi, S. Mathy, P. Desjardins, J. Elion, and E. Denamur. 1998. Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J. Infect. Dis. 177:642-650.

Bingen-Bidois, M., O. Clermont, S. Bonacorsi, M. Terki, N. Brahimi, C. Loukil, D. Barraud, and E. Bingen. 2002. Phylogenetic analysis and prevalence of urosepsis strains of Escherichia coli strains bearing pathogenicity islands-like domains. Infect. Immun. 70:3216-3226.

Blanc-Potard, A.-B., C. Tinsley, I. Scaletsky, C. Le Bouguenec, J. Guignot, A. L. Servin, X. Nassif, and M.-F. Bernet-Camard. 2002. Representational difference analysis between Afa/Dr diffusely adhering Escherichia coli and non-pathogenic E. coli K-12. Infect. Immun. 70:5503-5511.

Bonacorsi S., O. Clermont, V. Houdoin, C. Cordevant, N. Brahimi, A. Marecat, C. Tinsley, X. Nassif, M. Lange, and E. Bingen. 2003. Molecular analysis and experimental virulence of French and North American Escherichia coli neonatal meningitis isolates: identification of a new virulent clone. J. Infect. Dis. 187:1895-1906.

Clermont, O., S. Bonacorsi, and E. Bingen. 2000. Rapid and simple determination of the Escherichia coli phylogenetic groups. Appl. Environ. Microbiol. 66:4555-4558.

Escobar-Páramo, P., C. Giudicelli, C. Parsot, and E. Denamur. 2003. The evolutionary history of Shigella and enteroinvasive Escherichia coli revised. J. Mol. Evol. 57:140-148.

Escobar-Páramo, P., A. Sabbagh, P. Darlu, O. Pradillon, C. Vaury, G. Lecointre, and E. Denamur. Decreasing the effects of horizontal gene transfer on bacterial phylogeny: the Escherichia coli case study. Mol. Phylogenet. Evol. in press.

Germani, Y., E. Begaud, and C. Le Bouguenec. 1997. Detection of the Escherichia coli attaching and effacing gene (eaeA) as in enteropathogenic strains by polymerase chain reaction. Res. Microbiol. 148:177-181.

Guttman, D. S., and D.E. Dykhuizen. 1994. Detecting selective sweeps in naturally occurring Escherichia coli. Genetics 138:993-1003.

Johnson, J. R., and J. J. Brown. 1996. A novel multiply-primed polymerase chain reaction assay for identification of variant papG genes encoding the Gal (a1-4)Gal-binding PapG adhesins of Escherichia coli. J. Infect. Dis. 173:920-926.

Johnson, J. R., and A. L. Stell. 2000. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis. 181:261-272.

Le Bouguenec, C., M. Archambaud, and A. Labigne. 1992. Rapid and specific detection of the pap, afa, and sfa adhesin-encoding operons in uropathogenic Escherichia coli strains by polymerase chain reaction. J. Clin. Microbiol. 30:1189-1193.

Picard, B., P. Duriez, S. Gouriou, I. Matic, E. Denamur, and F. Taddei. 2001. Mutator natural Escherichia coli isolates have an unusual virulence phenotype. Infect. Immun. 69:9-14.

Pollard, D. R., W. M. Johnson, H. Lior, S. D. Tyler, and K. R. Rozee. 1990. Rapid and specific detection of verotoxin genes in Escherichia coli by polymerase chain reaction. J. Clin. Microbiol. 28:540-545.

Schmith, H., L. Beutin, and H. Karch. 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63:1055-1061.

Tornieporth, N. G., J. John, K. Salgado, P. de Jesus, E. Latham, M. C. Melo, S. T. Gunzburg, and L. W. Riley. 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J. Clin. Microbiol. 33:1371-1374.

Table S3: Extraintestinal virulence genotypes of studied strains and their PAI-like content

Strains

Phylo group

sfa/focDE

Adhesin type

iroN

iucC

papC

papG

allele

hlyCA

cnf1

hra

PAI-like type*

17-2

A

-

-

+

+

II

+

-

-

PAI ICFT073

ECOR24

A

-

-

+

+

II

+

-

+

PAI ICFT073

DEC9a

A

-

-

-

-

-

+

-

+

248/1-2

B1

-

+

-

+

-

-

-

+

ECOR58

B1

+

foc

+

-

-

-

-

-

-

PAI III536

DAECT179

C

-

-

+

+

III

+

+

+

PAI IIJ96

DEC7a

C

-

-

-

-

-

+

-

-

ECOR50

D

-

-

+

+

II

-

-

+

ECOR49

D

-

-

+

+

II

-

-

-

ECOR46

D

-

-

-

+

III

-

-

+

DAEC162

D

-

-

-

+

-

-

-

-

ECOR40

D

-

-

+

+

II

-

-

-

ECOR41

D

-

-

+

+

II

-

-

-

ECOR60

B2

+

foc

+

-

+

III

+

+

+

PAI III536 + PAI IIJ96

ECOR51

B2

+

foc

+

+

+

III

+

+

+


ECOR52

B2

+

foc

+

-

+

III

+

+

+


CFT073

B2

+

foc

+

+

+

II

+

-

-

PAI III536 + PAI ICFT073

ECOR57

B2

+

foc

+

+

+

II

-

-

-

PAI III536

ECOR62

B2

-

+

+

+

II

-

-

-

RS218

B2

+

sfa

+

-

+

III

+

+

+


ECOR64

B2

+

foc

+

-

-

-

-

-

-

PAI III536

EC7372

B2

-

-

+

+

II

+

-

-

PAI ICFT073

* PAI-like types were defined by simultaneous identification of different characteristic virulence factors such as sfa/foc and iroN (PAI III536); papGII, hly and iucC (PAI ICFT073); and hly, cnf1 and hra with or without pap (PAI IIJ96) (Bonacorsi et al. 2003)

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