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. 2015 Aug 19;370(1675):20140295.
doi: 10.1098/rstb.2014.0295.

Interactions between multiple helminths and the gut microbiota in wild rodents

Jakub Kreisinger  1 , Géraldine Bastien  1 , Heidi C Hauffe  1 , Julian Marchesi  2 , Sarah E Perkins  3
Affiliations

Interactions between multiple helminths and the gut microbiota in wild rodents

Jakub Kreisinger et al. Philos Trans R Soc Lond B Biol Sci. .

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.

Keywords: Apodemus flavicollis; community interactions; infracommunity; metagenome; wildlife microbiota.

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Figures

Figure 1.
Figure 1.
Mean proportions of reads of bacterial (a) phyla and (b) classes in 29 A. flavicollis infected and uninfected by the three most common helminths (Hymenolepis spp., Syphacia spp. and H. polygyrus).
Figure 2.
Figure 2.
Ordination plots for the overall association between gut microbiota content variation and the presence of three common helminths using (a) Bray–Curtis and (b) weighted UniFrac dissimilarities as the response variable (both analyses are controlled for variability in gut microbiota between different gut sections and geographical locations). Distribution of samples along the first two db-RDA axes (i.e. CAP1 and CAP2) and associated proportion of variation are shown. The presence of individual helminths is indicated by the coloured segments surrounding the data points (see the figure key). The length of the arrow indicates the relative importance of each helminth; bold arrows indicate a significant effect (all partial effects of individual helminths were significant; permutation-based p < 0.05).
Figure 3.
Figure 3.
Bootstrapped hierarchical clustering of log 2-fold change vectors for three common helminths (Syphacia spp., H. polygyrus and Hymenolepis spp.) in five gut sections. Log 2-fold change vectors characterize gut microbiota modulation induced by the presence of a particular helminth in different gut sections. Proximity in the dendrogram indicates a similar response and the scale of y-axis corresponds to distances among log 2-fold change vectors. Approximate unbiased (arb. units, in black) and bootstrap probability values (bp, in grey) are reported above individual nodes.
Figure 4.
Figure 4.
Heatmap of log 2-fold changes of OTUs that were significantly associated with the presence of at least one of the three common helminths (Syphacia spp., H. polygyrus and Hymenolepis spp.) in at least one gut section after DESeq2 analyses. Negative (blue) and positive (red) values indicate a decrease or increase, respectively, of a given OTU owing to the presence of a given helminth. Dendrogram on left-hand side: OTUs were grouped in two clusters according to Euclidean distances between associated log 2-fold changes and a Ward algorithm (see main text for more details). OTU identifications and their taxonomic assignations are listed on the right-hand side.
Figure 5.
Figure 5.
Ordination plots of the association between predicted metagenomic content and helminth presence, based on Bray–Curtis dissimilarities. Distribution of samples along the first two db-RDA axes (i.e. CAP1 and CAP2) and associated proportion of variation are shown. The presence of individual helminths is indicated by coloured segments surrounding the data points (see the figure key). Significant effects of the helminths are indicated by bold arrows (permutation-based p < 0.05).
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