Abstract

The gut microbiota is vital to host health and, as such, it is important to elucidate the mechanisms altering its composition and diversity. Intestinal helminths are host immunomodulators and have evolved both temporally and spatially in close association with the gut microbiota, resulting in potential mechanistic interplay. Host–helminth and host–microbiota interactions are comparatively well-examined, unlike microbiota–helminth relationships, which typically focus on experimental infection with a single helminth species in laboratory animals. Here, in addition to a review of the literature on helminth–microbiota interactions, we examined empirically the association between microbiota diversity and composition and natural infection of multiple helminth species in wild mice (Apodemus flavicollis), using 16S rRNA gene catalogues (metataxonomics). In general, helminth presence is linked with high microbiota diversity, which may confer health benefits to the host. Within our wild rodent system variation in the composition and abundance of gut microbial taxa associated with helminths was specific to each helminth species and occurred both up- and downstream of a given helminth's niche (gut position). The most pronounced helminth–microbiota association was between the presence of tapeworms in the small intestine and increased S24–7 (Bacteroidetes) family in the stomach. Helminths clearly have the potential to alter gut homeostasis. Free-living rodents with a diverse helminth community offer a useful model system that enables both correlative (this study) and manipulative inference to elucidate helminth–microbiota interactions.

Highlights

  • Mammals have coevolved with their gut microbial community for approximately 500 million years [1,2]

  • Within the gastrointestinal tract of 29 A. flavicollis, two helminth species (T. muris and Aspiculuris tetraptera) were present in only one individual, so these helminths were excluded from further analyses

  • Transmission routes to the host for each of the helminth species is via ingestion, life cycles differ between species such that Hymenolepis spp. and M. muris are acquired via ingestion of an insect intermediate host while H. polygyrus is acquired as infectious larvae and Syphacia spp. as infectious eggs

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Summary

Introduction

Mammals have coevolved with their gut microbial community (microbiota) for approximately 500 million years [1,2]. Changes in the composition of host microbiota owing to experimental infection with the nematode Trichuris suis has been observed in domesticated pigs [24], while experimental inoculation of laboratory mice with the common laboratory model nematode Heligmosomoides polygyrus bakeri has been associated with an increase in bacterial abundance at the site of helminth colonization, the ileum/small intestine [10], as well as within the caecum and colon [20].

Results
Conclusion

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