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Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization

Vaccination-induced Escherichia coli O157:H7-specific immune responses have been shown to reduce E. coli O157:H7 shedding in cattle. Although E. coli O157:H7 colonization is correlated with perturbations in intestinal microbial diversity, it is not yet known whether vaccination against E. coli O157:...

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Autores principales: Mir, Raies A., Schaut, Robert G., Allen, Heather K., Looft, Torey, Loving, Crystal L., Kudva, Indira T., Sharma, Vijay K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894827/
https://www.ncbi.nlm.nih.gov/pubmed/31805148
http://dx.doi.org/10.1371/journal.pone.0226099
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author Mir, Raies A.
Schaut, Robert G.
Allen, Heather K.
Looft, Torey
Loving, Crystal L.
Kudva, Indira T.
Sharma, Vijay K.
author_facet Mir, Raies A.
Schaut, Robert G.
Allen, Heather K.
Looft, Torey
Loving, Crystal L.
Kudva, Indira T.
Sharma, Vijay K.
author_sort Mir, Raies A.
collection PubMed
description Vaccination-induced Escherichia coli O157:H7-specific immune responses have been shown to reduce E. coli O157:H7 shedding in cattle. Although E. coli O157:H7 colonization is correlated with perturbations in intestinal microbial diversity, it is not yet known whether vaccination against E. coli O157:H7 could cause shifts in bovine intestinal microbiota. To understand the impact of E. coli O157:H7 vaccination and colonization on intestinal microbial diversity, cattle were vaccinated with two doses of different E. coli O157:H7 vaccine formulations. Six weeks post-vaccination, the two vaccinated groups (Vx-Ch) and one non-vaccinated group (NonVx-Ch) were orally challenged with E. coli O157:H7. Another group was neither vaccinated nor challenged (NonVx-NonCh). Fecal microbiota analysis over a 30-day period indicated a significant (FDR corrected, p <0.05) association of bacterial community structure with vaccination until E. coli O157:H7 challenge. Shannon diversity index and species richness were significantly lower in vaccinated compared to non-vaccinated groups after E. coli O157:H7 challenge (p < 0.05). The Firmicutes:Bacteroidetes ratio (p > 0.05) was not associated with vaccination but the relative abundance of Proteobacteria was significantly lower (p < 0.05) in vaccinated calves after E. coli O157:H7 challenge. Similarly, Vx-Ch calves had higher relative abundance of Paeniclostridium spp. and Christenellaceae R7 group while Campylobacter spp., and Sutterella spp. were more abundant in NonVx-Ch group post-E. coli O157:H7 challenge. Only Vx-Ch calves had significantly higher (p < 0.001) E. coli O157:H7-specific serum IgG but no detectable E. coli O157:H7-specific IgA. However, E. coli O157:H7-specific IL-10-producing T cells were detected in vaccinated animals prior to challenge, but IFN-γ-producing T cells were not detected. Neither E. coli O157:H7-specific IgG nor IgA were detected in blood or feces, respectively, of NonVx-Ch and NonVx-NonCh groups prior to or post vaccinations. Both Vx-Ch and NonVx-Ch animals shed detectable levels of challenge strain during the course of the study. Despite the lack of protection with the vaccine formulations there were detectable shifts in the microbiota of vaccinated animals before and after challenge with E. coli O157:H7.
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spelling pubmed-68948272019-12-14 Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization Mir, Raies A. Schaut, Robert G. Allen, Heather K. Looft, Torey Loving, Crystal L. Kudva, Indira T. Sharma, Vijay K. PLoS One Research Article Vaccination-induced Escherichia coli O157:H7-specific immune responses have been shown to reduce E. coli O157:H7 shedding in cattle. Although E. coli O157:H7 colonization is correlated with perturbations in intestinal microbial diversity, it is not yet known whether vaccination against E. coli O157:H7 could cause shifts in bovine intestinal microbiota. To understand the impact of E. coli O157:H7 vaccination and colonization on intestinal microbial diversity, cattle were vaccinated with two doses of different E. coli O157:H7 vaccine formulations. Six weeks post-vaccination, the two vaccinated groups (Vx-Ch) and one non-vaccinated group (NonVx-Ch) were orally challenged with E. coli O157:H7. Another group was neither vaccinated nor challenged (NonVx-NonCh). Fecal microbiota analysis over a 30-day period indicated a significant (FDR corrected, p <0.05) association of bacterial community structure with vaccination until E. coli O157:H7 challenge. Shannon diversity index and species richness were significantly lower in vaccinated compared to non-vaccinated groups after E. coli O157:H7 challenge (p < 0.05). The Firmicutes:Bacteroidetes ratio (p > 0.05) was not associated with vaccination but the relative abundance of Proteobacteria was significantly lower (p < 0.05) in vaccinated calves after E. coli O157:H7 challenge. Similarly, Vx-Ch calves had higher relative abundance of Paeniclostridium spp. and Christenellaceae R7 group while Campylobacter spp., and Sutterella spp. were more abundant in NonVx-Ch group post-E. coli O157:H7 challenge. Only Vx-Ch calves had significantly higher (p < 0.001) E. coli O157:H7-specific serum IgG but no detectable E. coli O157:H7-specific IgA. However, E. coli O157:H7-specific IL-10-producing T cells were detected in vaccinated animals prior to challenge, but IFN-γ-producing T cells were not detected. Neither E. coli O157:H7-specific IgG nor IgA were detected in blood or feces, respectively, of NonVx-Ch and NonVx-NonCh groups prior to or post vaccinations. Both Vx-Ch and NonVx-Ch animals shed detectable levels of challenge strain during the course of the study. Despite the lack of protection with the vaccine formulations there were detectable shifts in the microbiota of vaccinated animals before and after challenge with E. coli O157:H7. Public Library of Science 2019-12-05 /pmc/articles/PMC6894827/ /pubmed/31805148 http://dx.doi.org/10.1371/journal.pone.0226099 Text en https://creativecommons.org/publicdomain/zero/1.0/ This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Mir, Raies A.
Schaut, Robert G.
Allen, Heather K.
Looft, Torey
Loving, Crystal L.
Kudva, Indira T.
Sharma, Vijay K.
Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization
title Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization
title_full Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization
title_fullStr Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization
title_full_unstemmed Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization
title_short Cattle intestinal microbiota shifts following Escherichia coli O157:H7 vaccination and colonization
title_sort cattle intestinal microbiota shifts following escherichia coli o157:h7 vaccination and colonization
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894827/
https://www.ncbi.nlm.nih.gov/pubmed/31805148
http://dx.doi.org/10.1371/journal.pone.0226099
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