Abstract

Parasitic nematodes are potent modulators of immune reactivity in mice and men. Intestinal nematodes live in close contact with commensal gut bacteria, provoke biased Th2 immune responses upon infection, and subsequently lead to changes in gut physiology. We hypothesized that murine nematode infection is associated with distinct changes of the intestinal bacterial microbiota composition. We here studied intestinal inflammatory and immune responses in mice following infection with the hookworm Heligmosomoidespolygyrus bakeri and applied cultural and molecular techniques to quantitatively assess intestinal microbiota changes in the ileum, cecum and colon. At day 14 post nematode infection, mice harbored significantly higher numbers of γ-Proteobacteria/Enterobacteriaceae and members of the Bacteroides /Prevotella group in their cecum as compared to uninfected controls. Abundance of Gram-positive species such as Lactobacilli, Clostridia as well as the total bacterial load was not affected by worm infection. The altered microbiota composition was independent of the IL-4/-13 – STAT6 signaling axis, as infected IL-4Rα-/- mice showed a similar increase in enterobacterial loads. In conclusion, infection with an enteric nematode is accompanied by distinct intestinal microbiota changes towards higher abundance of gram-negative commensal species at the small intestinal site of infection (and inflammation), but also in the parasite-free large intestinal tract. Further studies should unravel the impact of nematode-induced microbiota changes in inflammatory bowel disease to allow for a better understanding of how theses parasites interfere with intestinal inflammation and bacterial communities in men.

Highlights

  • Nematodes are the most prevalent worms worldwide dwelling the intestine of humans

  • Parasitic nematodes are considered as a therapeutic option for the treatment of inflammatory bowel disease (IBD) [7] given that trials applying helminth eggs to patients with Crohn’s disease and ulcerative colitis resulted in disease remission [8]

  • In the present study we analyzed whether infection with the nematode H. p. bakeri dwelling the proximal small intestine and the subsequently induced immune responses are associated with distinct changes of the intestinal bacterial microbiota composition

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Summary

Introduction

Nematodes are the most prevalent worms worldwide dwelling the intestine of humans. Infections with Ascaris lumbricoides, Trichuris trichura, Ancylostoma duodenale and Necator americanus generally lead to persistent intestinal colonization [1]. Enteropathogenic infections and murine experimental colitis lead to dramatic changes in the intestinal ecosystem with alterations in the microbiota composition [10] These models reflect a multifactorial etiology of intestinal inflammation, the resulting changes in the composition of the intestinal microbial community are consistently seen as a preferential overgrowth of the Gramnegative Enterobacteriaceae. It is under debate whether the phenomenon of “dysbiosis” in animal models and human IBD is primarily resulting from intestinal inflammation or initiating and perpetuating the inflammatory condition per se (“hen and egg”) [11,12,13]

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