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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

Authors
  • Myhill, Laura J.1
  • Stolzenbach, Sophie1
  • Mejer, Helena1
  • Krych, Lukasz2
  • Jakobsen, Simon R.1
  • Kot, Witold3
  • Skovgaard, Kerstin4
  • Canibe, Nuria5
  • Nejsum, Peter6
  • Nielsen, Dennis S.2
  • Thamsborg, Stig M.1
  • Williams, Andrew R.1
  • 1 Department of Veterinary and Animal Sciences, University of Copenhagen, Faculty of Health and Medical Sciences, Frederiksberg , (Denmark)
  • 2 Department of Food Science, University of Copenhagen, Frederiksberg , (Denmark)
  • 3 Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg , (Denmark)
  • 4 Department of Biotechnology and Biomedicine, Technical University of Denmark, Kongens Lyngby , (Denmark)
  • 5 Department of Animal Science – Immunology and Microbiology, Aarhus University, Tjele , (Denmark)
  • 6 Department of Clinical Medicine, Aarhus University, Aarhus , (Denmark)
Type
Published Article
Journal
Frontiers in Immunology
Publisher
Frontiers Media SA
Publication Date
Jan 05, 2022
Volume
12
Identifiers
DOI: 10.3389/fimmu.2021.793260
Source
Frontiers
Keywords
Disciplines
  • Immunology
  • Original Research
License
Green

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.

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