Cargando…
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...
Autores principales: | , , , , , , , , , , , |
---|---|
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 |
_version_ | 1784634569997156352 |
---|---|
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. |
format | Online Article Text |
id | pubmed-8766631 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT myhilllauraj parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT stolzenbachsophie parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT mejerhelena parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT krychlukasz parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT jakobsensimonr parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT kotwitold parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT skovgaardkerstin parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT canibenuria parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT nejsumpeter parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT nielsendenniss parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT thamsborgstigm parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection AT williamsandrewr parasiteprobioticinteractionsinthegutbacillusspandenterococcusfaeciumregulatetype2inflammatoryresponsesandmodifythegutmicrobiotaofpigsduringhelminthinfection |