Genetic relatedness and virulence properties of enteropathogenic Escherichia coli strains of serotype O119: H6 expressing localized adherence or localized and aggregative adherence-like patterns on HeLa cells

Bruna G. Garcia, Tadasuke Ooka, Yasuhiro Gotoh, Mônica A.M. Vieira, Denise Yamamoto, Yoshitoshi Ogura, Dennys M. Girão, Suely C.F. Sampaio, Alexis Bonfim Melo, Kinue Irino, Tetsuya Hayashi, Tânia A.T. Gomes

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Abstract

Enteropathogenic Escherichia coli (EPEC) induce attaching and effacing (A/E) lesions in enterocytes and produce the bundle-forming pilus (BFP) contributing to the localized adherence (LA) pattern formation on HeLa cells. Enteroaggregative E. coli (EAEC) produce aggregative adherence (AA) on HeLa cells and form prominent biofilms. The ability to produce LA or AA is an important hallmark to classify fecal E. coli isolates as EPEC or EAEC, respectively. E. coli strains of serotype O119:H6 exhibit an LA+ phenotype and have been considered as comprising a clonal group. of EPEC strains. However, we have recently identified O119:H6 EPEC strains that produce LA and an AA-like pattern concurrently (LA/AA-like+). In this study, we evaluated the relatedness of three LA/AA-like+ and three LA+ O119:H6 strains by comparing their virulence and genotypic properties. We first found that the LA/AA-like+ strains induced actin accumulation in HeLa cells (indicative of A/E lesions formation) and formed biofilms on abiotic surfaces more efficiently than the LA+ strains. MLST analysis showed that the six strains all belong to the ST28 complex. All strains carried multiple plasmids, but as plasmid profiles were highly variable, this cannot be used to differentiate LA/AA-like+ and LA+ strains. We further obtained their draft genome sequences and the complete sequences of four plasmids harbored by one LA/AA-like+ strain. Analysis of these sequences and comparison with 37 fully sequenced E. coli genomes revealed that both O119:H6 groups belong to the E. coli phylogroup B2 and are very closely related with only 58-67 SNPs found between LA/AA-like+ and LA+ strains. Search of the draft sequences of the six strains for adhesion-related genes known in EAEC and other E. coli pathotypes detected no genes specifically present in LA/AA-like+ strains. Unexpectedly however, we found that a large plasmid distinct from pEAF is responsible for the AA-like phenotype of the LA/AA-like+ strains. Although we have not identified any plasmid genes specifically present in all LA/AA-like+ strains and absent in the LA+ strains, these results suggest the presence of an unknown mechanism to promote the AA-like pattern production and biofilm formation by the LA/AA-like+ strains. Because their ability to produce A/E lesions and biofilm concomitantly could exacerbate the clinical condition of the patient and lead to persistent diarrhea, the mechanism underlying the enhanced biofilm formation by the LA/AA-like+ O119:H6 strains and their spread and involvement in severe diarrheal diseases should be more intensively investigated.

Original languageEnglish
Pages (from-to)152-164
Number of pages13
JournalInternational Journal of Medical Microbiology
Volume306
Issue number3
DOIs
Publication statusPublished - May 1 2016

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Enteropathogenic Escherichia coli
HeLa Cells
Virulence
Escherichia coli
Biofilms
Plasmids
Genome
Genes
Phenotype
Serogroup
Enterocytes
Single Nucleotide Polymorphism
Sequence Analysis
Actins
Diarrhea

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Microbiology (medical)
  • Infectious Diseases

Cite this

Genetic relatedness and virulence properties of enteropathogenic Escherichia coli strains of serotype O119 : H6 expressing localized adherence or localized and aggregative adherence-like patterns on HeLa cells. / Garcia, Bruna G.; Ooka, Tadasuke; Gotoh, Yasuhiro; Vieira, Mônica A.M.; Yamamoto, Denise; Ogura, Yoshitoshi; Girão, Dennys M.; Sampaio, Suely C.F.; Melo, Alexis Bonfim; Irino, Kinue; Hayashi, Tetsuya; Gomes, Tânia A.T.

In: International Journal of Medical Microbiology, Vol. 306, No. 3, 01.05.2016, p. 152-164.

Research output: Contribution to journalArticle

Garcia, Bruna G. ; Ooka, Tadasuke ; Gotoh, Yasuhiro ; Vieira, Mônica A.M. ; Yamamoto, Denise ; Ogura, Yoshitoshi ; Girão, Dennys M. ; Sampaio, Suely C.F. ; Melo, Alexis Bonfim ; Irino, Kinue ; Hayashi, Tetsuya ; Gomes, Tânia A.T. / Genetic relatedness and virulence properties of enteropathogenic Escherichia coli strains of serotype O119 : H6 expressing localized adherence or localized and aggregative adherence-like patterns on HeLa cells. In: International Journal of Medical Microbiology. 2016 ; Vol. 306, No. 3. pp. 152-164.
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abstract = "Enteropathogenic Escherichia coli (EPEC) induce attaching and effacing (A/E) lesions in enterocytes and produce the bundle-forming pilus (BFP) contributing to the localized adherence (LA) pattern formation on HeLa cells. Enteroaggregative E. coli (EAEC) produce aggregative adherence (AA) on HeLa cells and form prominent biofilms. The ability to produce LA or AA is an important hallmark to classify fecal E. coli isolates as EPEC or EAEC, respectively. E. coli strains of serotype O119:H6 exhibit an LA+ phenotype and have been considered as comprising a clonal group. of EPEC strains. However, we have recently identified O119:H6 EPEC strains that produce LA and an AA-like pattern concurrently (LA/AA-like+). In this study, we evaluated the relatedness of three LA/AA-like+ and three LA+ O119:H6 strains by comparing their virulence and genotypic properties. We first found that the LA/AA-like+ strains induced actin accumulation in HeLa cells (indicative of A/E lesions formation) and formed biofilms on abiotic surfaces more efficiently than the LA+ strains. MLST analysis showed that the six strains all belong to the ST28 complex. All strains carried multiple plasmids, but as plasmid profiles were highly variable, this cannot be used to differentiate LA/AA-like+ and LA+ strains. We further obtained their draft genome sequences and the complete sequences of four plasmids harbored by one LA/AA-like+ strain. Analysis of these sequences and comparison with 37 fully sequenced E. coli genomes revealed that both O119:H6 groups belong to the E. coli phylogroup B2 and are very closely related with only 58-67 SNPs found between LA/AA-like+ and LA+ strains. Search of the draft sequences of the six strains for adhesion-related genes known in EAEC and other E. coli pathotypes detected no genes specifically present in LA/AA-like+ strains. Unexpectedly however, we found that a large plasmid distinct from pEAF is responsible for the AA-like phenotype of the LA/AA-like+ strains. Although we have not identified any plasmid genes specifically present in all LA/AA-like+ strains and absent in the LA+ strains, these results suggest the presence of an unknown mechanism to promote the AA-like pattern production and biofilm formation by the LA/AA-like+ strains. Because their ability to produce A/E lesions and biofilm concomitantly could exacerbate the clinical condition of the patient and lead to persistent diarrhea, the mechanism underlying the enhanced biofilm formation by the LA/AA-like+ O119:H6 strains and their spread and involvement in severe diarrheal diseases should be more intensively investigated.",
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T2 - H6 expressing localized adherence or localized and aggregative adherence-like patterns on HeLa cells

AU - Garcia, Bruna G.

AU - Ooka, Tadasuke

AU - Gotoh, Yasuhiro

AU - Vieira, Mônica A.M.

AU - Yamamoto, Denise

AU - Ogura, Yoshitoshi

AU - Girão, Dennys M.

AU - Sampaio, Suely C.F.

AU - Melo, Alexis Bonfim

AU - Irino, Kinue

AU - Hayashi, Tetsuya

AU - Gomes, Tânia A.T.

PY - 2016/5/1

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N2 - Enteropathogenic Escherichia coli (EPEC) induce attaching and effacing (A/E) lesions in enterocytes and produce the bundle-forming pilus (BFP) contributing to the localized adherence (LA) pattern formation on HeLa cells. Enteroaggregative E. coli (EAEC) produce aggregative adherence (AA) on HeLa cells and form prominent biofilms. The ability to produce LA or AA is an important hallmark to classify fecal E. coli isolates as EPEC or EAEC, respectively. E. coli strains of serotype O119:H6 exhibit an LA+ phenotype and have been considered as comprising a clonal group. of EPEC strains. However, we have recently identified O119:H6 EPEC strains that produce LA and an AA-like pattern concurrently (LA/AA-like+). In this study, we evaluated the relatedness of three LA/AA-like+ and three LA+ O119:H6 strains by comparing their virulence and genotypic properties. We first found that the LA/AA-like+ strains induced actin accumulation in HeLa cells (indicative of A/E lesions formation) and formed biofilms on abiotic surfaces more efficiently than the LA+ strains. MLST analysis showed that the six strains all belong to the ST28 complex. All strains carried multiple plasmids, but as plasmid profiles were highly variable, this cannot be used to differentiate LA/AA-like+ and LA+ strains. We further obtained their draft genome sequences and the complete sequences of four plasmids harbored by one LA/AA-like+ strain. Analysis of these sequences and comparison with 37 fully sequenced E. coli genomes revealed that both O119:H6 groups belong to the E. coli phylogroup B2 and are very closely related with only 58-67 SNPs found between LA/AA-like+ and LA+ strains. Search of the draft sequences of the six strains for adhesion-related genes known in EAEC and other E. coli pathotypes detected no genes specifically present in LA/AA-like+ strains. Unexpectedly however, we found that a large plasmid distinct from pEAF is responsible for the AA-like phenotype of the LA/AA-like+ strains. Although we have not identified any plasmid genes specifically present in all LA/AA-like+ strains and absent in the LA+ strains, these results suggest the presence of an unknown mechanism to promote the AA-like pattern production and biofilm formation by the LA/AA-like+ strains. Because their ability to produce A/E lesions and biofilm concomitantly could exacerbate the clinical condition of the patient and lead to persistent diarrhea, the mechanism underlying the enhanced biofilm formation by the LA/AA-like+ O119:H6 strains and their spread and involvement in severe diarrheal diseases should be more intensively investigated.

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