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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-01-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.793260/full |
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| author | Laura J. Myhill Sophie Stolzenbach Helena Mejer Lukasz Krych Simon R. Jakobsen Witold Kot Kerstin Skovgaard Nuria Canibe Peter Nejsum Dennis S. Nielsen Stig M. Thamsborg Andrew R. Williams |
| author_facet | Laura J. Myhill Sophie Stolzenbach Helena Mejer Lukasz Krych Simon R. Jakobsen Witold Kot Kerstin Skovgaard Nuria Canibe Peter Nejsum Dennis S. Nielsen Stig M. Thamsborg Andrew R. Williams |
| author_sort | Laura J. Myhill |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-24T01:37:54Z |
| format | Article |
| id | doaj.art-1bb98401c45243d5a25b80568ff3ea19 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-24T01:37:54Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-1bb98401c45243d5a25b80568ff3ea192022-12-21T17:22:08ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-01-011210.3389/fimmu.2021.793260793260Parasite-Probiotic Interactions in the Gut: Bacillus sp. and Enterococcus faecium Regulate Type-2 Inflammatory Responses and Modify the Gut Microbiota of Pigs During Helminth InfectionLaura J. Myhill0Sophie Stolzenbach1Helena Mejer2Lukasz Krych3Simon R. Jakobsen4Witold Kot5Kerstin Skovgaard6Nuria Canibe7Peter Nejsum8Dennis S. Nielsen9Stig M. Thamsborg10Andrew R. Williams11Department of Veterinary and Animal Sciences, University of Copenhagen, Faculty of Health and Medical Sciences, Frederiksberg, DenmarkDepartment of Veterinary and Animal Sciences, University of Copenhagen, Faculty of Health and Medical Sciences, Frederiksberg, DenmarkDepartment of Veterinary and Animal Sciences, University of Copenhagen, Faculty of Health and Medical Sciences, Frederiksberg, DenmarkDepartment of Food Science, University of Copenhagen, Frederiksberg, DenmarkDepartment of Veterinary and Animal Sciences, University of Copenhagen, Faculty of Health and Medical Sciences, Frederiksberg, DenmarkDepartment of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg, DenmarkDepartment of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby, DenmarkDepartment of Animal Science – Immunology and Microbiology, Aarhus University, Tjele, DenmarkDepartment of Clinical Medicine, Aarhus University, Aarhus, DenmarkDepartment of Food Science, University of Copenhagen, Frederiksberg, DenmarkDepartment of Veterinary and Animal Sciences, University of Copenhagen, Faculty of Health and Medical Sciences, Frederiksberg, DenmarkDepartment of Veterinary and Animal Sciences, University of Copenhagen, Faculty of Health and Medical Sciences, Frederiksberg, DenmarkDietary 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.https://www.frontiersin.org/articles/10.3389/fimmu.2021.793260/fullprobioticsswinehelminthsOesophagostomum dentatumtype-2 immune responsegut microbiota |
| spellingShingle | Laura J. Myhill Sophie Stolzenbach Helena Mejer Lukasz Krych Simon R. Jakobsen Witold Kot Kerstin Skovgaard Nuria Canibe Peter Nejsum Dennis S. Nielsen Stig M. Thamsborg Andrew R. Williams 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 Frontiers in Immunology probiotics swine helminths Oesophagostomum dentatum type-2 immune response gut microbiota |
| 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 | probiotics swine helminths Oesophagostomum dentatum type-2 immune response gut microbiota |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.793260/full |
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