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Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection

Dietary probiotics may enhance gut health by directly competing with pathogenic agents and through immunostimulatory effects. These properties are recognized in the context of bacterial and viral pathogens, but less is known about interactions with eukaryotic pathogens such as parasitic worms (helmi...

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Autores principales: Myhill, Laura J., Stolzenbach, Sophie, Mejer, Helena, Krych, Lukasz, Jakobsen, Simon R., Kot, Witold, Skovgaard, Kerstin, Canibe, Nuria, Nejsum, Peter, Nielsen, Dennis S., Thamsborg, Stig M., Williams, Andrew R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8766631/
https://www.ncbi.nlm.nih.gov/pubmed/35069576
http://dx.doi.org/10.3389/fimmu.2021.793260
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author Myhill, Laura J.
Stolzenbach, Sophie
Mejer, Helena
Krych, Lukasz
Jakobsen, Simon R.
Kot, Witold
Skovgaard, Kerstin
Canibe, Nuria
Nejsum, Peter
Nielsen, Dennis S.
Thamsborg, Stig M.
Williams, Andrew R.
author_facet Myhill, Laura J.
Stolzenbach, Sophie
Mejer, Helena
Krych, Lukasz
Jakobsen, Simon R.
Kot, Witold
Skovgaard, Kerstin
Canibe, Nuria
Nejsum, Peter
Nielsen, Dennis S.
Thamsborg, Stig M.
Williams, Andrew R.
author_sort Myhill, Laura J.
collection PubMed
description Dietary probiotics may enhance gut health by directly competing with pathogenic agents and through immunostimulatory effects. These properties are recognized in the context of bacterial and viral pathogens, but less is known about interactions with eukaryotic pathogens such as parasitic worms (helminths). In this study we investigated whether two probiotic mixtures (comprised of Bacillus amyloliquefaciens, B. subtilis, and Enterococcus faecium [BBE], or Lactobacillus rhamnosus LGG and Bifidobacterium animalis subspecies Lactis Bb12 [LB]) could modulate helminth infection kinetics as well as the gut microbiome and intestinal immune responses in pigs infected with the nodular worm Oesophagostomum dentatum. We observed that neither probiotic mixture influenced helminth infection levels. BBE, and to a lesser extent LB, changed the alpha- and beta-diversity indices of the colon and fecal microbiota, notably including an enrichment of fecal Bifidobacterium spp. by BBE. However, these effects were muted by concurrent O. dentatum infection. BBE (but not LB) significantly attenuated the O. dentatum-induced upregulation of genes involved in type-2 inflammation and restored normal lymphocyte ratios in the ileo-caecal lymph nodes that were altered by infection. Moreover, inflammatory cytokine release from blood mononuclear cells and intestinal lymphocytes was diminished by BBE. Collectively, our data suggest that selected probiotic mixtures can play a role in maintaining immune homeostasis during type 2-biased inflammation. In addition, potentially beneficial changes in the microbiome induced by dietary probiotics may be counteracted by helminths, highlighting the complex inter-relationships that potentially exist between probiotic bacteria and intestinal parasites.
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spelling pubmed-87666312022-01-20 Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection Myhill, Laura J. Stolzenbach, Sophie Mejer, Helena Krych, Lukasz Jakobsen, Simon R. Kot, Witold Skovgaard, Kerstin Canibe, Nuria Nejsum, Peter Nielsen, Dennis S. Thamsborg, Stig M. Williams, Andrew R. Front Immunol Immunology Dietary probiotics may enhance gut health by directly competing with pathogenic agents and through immunostimulatory effects. These properties are recognized in the context of bacterial and viral pathogens, but less is known about interactions with eukaryotic pathogens such as parasitic worms (helminths). In this study we investigated whether two probiotic mixtures (comprised of Bacillus amyloliquefaciens, B. subtilis, and Enterococcus faecium [BBE], or Lactobacillus rhamnosus LGG and Bifidobacterium animalis subspecies Lactis Bb12 [LB]) could modulate helminth infection kinetics as well as the gut microbiome and intestinal immune responses in pigs infected with the nodular worm Oesophagostomum dentatum. We observed that neither probiotic mixture influenced helminth infection levels. BBE, and to a lesser extent LB, changed the alpha- and beta-diversity indices of the colon and fecal microbiota, notably including an enrichment of fecal Bifidobacterium spp. by BBE. However, these effects were muted by concurrent O. dentatum infection. BBE (but not LB) significantly attenuated the O. dentatum-induced upregulation of genes involved in type-2 inflammation and restored normal lymphocyte ratios in the ileo-caecal lymph nodes that were altered by infection. Moreover, inflammatory cytokine release from blood mononuclear cells and intestinal lymphocytes was diminished by BBE. Collectively, our data suggest that selected probiotic mixtures can play a role in maintaining immune homeostasis during type 2-biased inflammation. In addition, potentially beneficial changes in the microbiome induced by dietary probiotics may be counteracted by helminths, highlighting the complex inter-relationships that potentially exist between probiotic bacteria and intestinal parasites. Frontiers Media S.A. 2022-01-05 /pmc/articles/PMC8766631/ /pubmed/35069576 http://dx.doi.org/10.3389/fimmu.2021.793260 Text en Copyright © 2022 Myhill, Stolzenbach, Mejer, Krych, Jakobsen, Kot, Skovgaard, Canibe, Nejsum, Nielsen, Thamsborg and Williams https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Myhill, Laura J.
Stolzenbach, Sophie
Mejer, Helena
Krych, Lukasz
Jakobsen, Simon R.
Kot, Witold
Skovgaard, Kerstin
Canibe, Nuria
Nejsum, Peter
Nielsen, Dennis S.
Thamsborg, Stig M.
Williams, Andrew R.
Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection
title Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection
title_full Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection
title_fullStr Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection
title_full_unstemmed Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection
title_short Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth Infection
title_sort parasite-probiotic interactions in the gut: bacillus sp. and enterococcus faecium regulate type-2 inflammatory responses and modify the gut microbiota of pigs during helminth infection
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8766631/
https://www.ncbi.nlm.nih.gov/pubmed/35069576
http://dx.doi.org/10.3389/fimmu.2021.793260
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