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

Laura J Myhill, Sophie Stolzenbach, Helena Mejer, Lukasz Krych, Simon R Jakobsen, Witold Kot, Kerstin Skovgaard, Nuria Canibe, Peter Lindberg Nejsum, Dennis S. Nielsen, Stig Milan Thamsborg, Andrew R Williams*

*Corresponding author for this work

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

Abstract

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.
Original languageEnglish
Article number793260
JournalFrontiers in Immunology
Volume12
Number of pages14
ISSN1664-3224
DOIs
Publication statusPublished - Jan 2022

Keywords

  • Oesophagostomum dentatum
  • gut microbiota
  • helminths
  • probiotics
  • swine
  • type-2 immune response
  • IMMUNE-RESPONSE
  • MIXTURE
  • OESOPHAGOSTOMUM-DENTATUM INFECTION
  • INULIN
  • GIARDIA-INTESTINALIS
  • SUPPLEMENTATION
  • INHIBITION
  • GROWTH
  • Bacillus/immunology
  • Male
  • Swine
  • Female
  • Probiotics/pharmacology
  • Enterococcus faecium/immunology
  • Swine Diseases/immunology
  • Oesophagostomum/immunology
  • Animals
  • Gastrointestinal Microbiome/immunology
  • Oesophagostomiasis/immunology

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