Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial Cells

Shiga toxin-producing, enterohemorrhagic Escherichia coli (EHEC) serotype O157:H7 is a major foodborne pathogen causing symptoms ranging from simple intestinal discomfort to bloody diarrhea and life-threatening hemolytic uremic syndrome in humans. Cattle can be asymptomatically colonized by O157:H7...

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Main Authors: Matthew R. Moreau, Indira T. Kudva, Robab Katani, Rebecca Cote, Lingling Li, Terrance M. Arthur, Vivek Kapur
Format: Article
Language:English
Published: Wiley 2021-01-01
Series:International Journal of Microbiology
Online Access:http://dx.doi.org/10.1155/2021/8868151
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author Matthew R. Moreau
Indira T. Kudva
Robab Katani
Rebecca Cote
Lingling Li
Terrance M. Arthur
Vivek Kapur
author_facet Matthew R. Moreau
Indira T. Kudva
Robab Katani
Rebecca Cote
Lingling Li
Terrance M. Arthur
Vivek Kapur
author_sort Matthew R. Moreau
collection DOAJ
description Shiga toxin-producing, enterohemorrhagic Escherichia coli (EHEC) serotype O157:H7 is a major foodborne pathogen causing symptoms ranging from simple intestinal discomfort to bloody diarrhea and life-threatening hemolytic uremic syndrome in humans. Cattle can be asymptomatically colonized by O157:H7 predominantly at the rectoanal junction (RAJ). Colonization of the RAJ is highly associated with the shedding of O157:H7 in bovine feces. Supershedding (SS) is a phenomenon that has been reported in some cattle that shed more than 104 colony-forming units of O57:H7 per gram of feces, 100–1000 times more or greater than normal shedders. The unique bovine RAJ cell adherence model revealed that O157:H7 employs a LEE-independent mechanism of attachment to one of the RAJ cell types, the squamous epithelial (RSE) cells. Nine nonfimbrial adhesins were selected to determine their role in the characteristic hyperadherent phenotype of SS O157 on bovine RSE cells, in comparison with human HEp-2 cells. A number of single nucleotide polymorphisms (SNPs) were found amongst these nonfimbrial adhesins across a number of SS isolates. In human cells, deletion of yfaL reduced the adherence of both EDL933 and SS17. However, deletion of eae resulted in a significant loss of adherence in SS17 whereas deletion of wzzB and iha in EDL933 resulted in the same loss of adherence to HEp-2 cells. On RSE cells, none of these nonfimbrial deletion mutants were able to alter the adherence phenotype of SS17. In EDL933, deletion of cah resulted in mitigated adherence. Surprisingly, four nonfimbrial adhesin gene deletions were actually able to confer the hyperadherent phenotype on RSE cells. Overall, this study reveals that the contribution of nonfimbrial adhesins to the adherence mechanisms and functions of O157:H7 is both strain and host cell type dependent as well as indicates a possible role of these nonfimbrial adhesins in the SS phenotype exhibited on RSE cells.
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spelling doaj-art-1ea2dcb9211a4387a1147c721e4c9a0e2025-02-03T01:05:05ZengWileyInternational Journal of Microbiology1687-918X1687-91982021-01-01202110.1155/2021/88681518868151Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial CellsMatthew R. Moreau0Indira T. Kudva1Robab Katani2Rebecca Cote3Lingling Li4Terrance M. Arthur5Vivek Kapur6Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA, USAFood Safety and Enteric Pathogens Research Unit, National Animal Disease Center, Agricultural Research Service, U.S. Department of Agriculture, Ames, IA, USADepartment of Animal Science, The Pennsylvania State University, University Park, PA, USADepartment of Veterinary and Biomedical Sciences, The Pennsylvania State University, University Park, PA, USADepartment of Animal Science, The Pennsylvania State University, University Park, PA, USARoman L. Hruska U.S. Mean Animal Research Center, Agricultural Research Service, U.S. Department of Agriculture, Clay Center, NE, USADepartment of Animal Science, The Pennsylvania State University, University Park, PA, USAShiga toxin-producing, enterohemorrhagic Escherichia coli (EHEC) serotype O157:H7 is a major foodborne pathogen causing symptoms ranging from simple intestinal discomfort to bloody diarrhea and life-threatening hemolytic uremic syndrome in humans. Cattle can be asymptomatically colonized by O157:H7 predominantly at the rectoanal junction (RAJ). Colonization of the RAJ is highly associated with the shedding of O157:H7 in bovine feces. Supershedding (SS) is a phenomenon that has been reported in some cattle that shed more than 104 colony-forming units of O57:H7 per gram of feces, 100–1000 times more or greater than normal shedders. The unique bovine RAJ cell adherence model revealed that O157:H7 employs a LEE-independent mechanism of attachment to one of the RAJ cell types, the squamous epithelial (RSE) cells. Nine nonfimbrial adhesins were selected to determine their role in the characteristic hyperadherent phenotype of SS O157 on bovine RSE cells, in comparison with human HEp-2 cells. A number of single nucleotide polymorphisms (SNPs) were found amongst these nonfimbrial adhesins across a number of SS isolates. In human cells, deletion of yfaL reduced the adherence of both EDL933 and SS17. However, deletion of eae resulted in a significant loss of adherence in SS17 whereas deletion of wzzB and iha in EDL933 resulted in the same loss of adherence to HEp-2 cells. On RSE cells, none of these nonfimbrial deletion mutants were able to alter the adherence phenotype of SS17. In EDL933, deletion of cah resulted in mitigated adherence. Surprisingly, four nonfimbrial adhesin gene deletions were actually able to confer the hyperadherent phenotype on RSE cells. Overall, this study reveals that the contribution of nonfimbrial adhesins to the adherence mechanisms and functions of O157:H7 is both strain and host cell type dependent as well as indicates a possible role of these nonfimbrial adhesins in the SS phenotype exhibited on RSE cells.http://dx.doi.org/10.1155/2021/8868151
spellingShingle Matthew R. Moreau
Indira T. Kudva
Robab Katani
Rebecca Cote
Lingling Li
Terrance M. Arthur
Vivek Kapur
Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial Cells
International Journal of Microbiology
title Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial Cells
title_full Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial Cells
title_fullStr Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial Cells
title_full_unstemmed Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial Cells
title_short Nonfimbrial Adhesin Mutants Reveal Divergent Escherichia coli O157:H7 Adherence Mechanisms on Human and Cattle Epithelial Cells
title_sort nonfimbrial adhesin mutants reveal divergent escherichia coli o157 h7 adherence mechanisms on human and cattle epithelial cells
url http://dx.doi.org/10.1155/2021/8868151
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