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Interactions between multiple helminths and the gut microbiota in wild rodents.

Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE - Philos. Trans. R. Soc. Lond., B, Biol. Sci. (2015)

Bottom Line: 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).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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biodiversity and Molecular Ecology, Centre for Research and Innovation, Fondazione Edmund Mach, Via E. Mach 1, 38010 S. Michele all'Adige, TN, Italy.

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.

No MeSH data available.


Related in: MedlinePlus

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).
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RSTB20140295F2: 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).

Mentions: Taxonomic assignment of OTUs to phylum and class level did not reveal any pronounced changes in community composition whether helminths were present or absent (figure 1). However, H. polygyrus presence was associated with a slight increase in the Firmicutes/Bacteroidetes ratio along the whole gut for infected individuals (mean ± s.e.: 23.151 ± 28.894 and 50.600 ± 10.398), although this effect was not significant (LME: Δd.f. = 1, χ2 = 2.747, p = 0.0974). Instead, constrained ordination (db-RDA) revealed the presence of any of the three common helminths to be associated with significant changes in whole-gut bacterial communities (table 2 and figure 2), although the effect size was low. Instead, Syphacia spp. are associated with a gut microbiota that is divergent, in terms of composition, to that associated with H. polygyrus (figure 2). By contrast, the community composition associated with Hymenolepis spp. was not associated with either of the other two common helminths, and these differences were consistent regardless of which distance index was used (figure 2). The variance, however, explained in the helminth-associated community composition was very low (adjusted R2 ranged between 0.004 and 0.016; table 2). Helminth abundance was also associated with significant changes in the overall microbiota composition, except for Hymenolepis spp. which was marginally non-significant (p = 0.079), although, again, the proportion of variance explained was still low (adjusted R2 ranged between 0.002 and 0.014; table 2)Table 2.


Interactions between multiple helminths and the gut microbiota in wild rodents.

Kreisinger J, Bastien G, Hauffe HC, Marchesi J, Perkins SE - Philos. Trans. R. Soc. Lond., B, Biol. Sci. (2015)

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).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4528493&req=5

RSTB20140295F2: 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).
Mentions: Taxonomic assignment of OTUs to phylum and class level did not reveal any pronounced changes in community composition whether helminths were present or absent (figure 1). However, H. polygyrus presence was associated with a slight increase in the Firmicutes/Bacteroidetes ratio along the whole gut for infected individuals (mean ± s.e.: 23.151 ± 28.894 and 50.600 ± 10.398), although this effect was not significant (LME: Δd.f. = 1, χ2 = 2.747, p = 0.0974). Instead, constrained ordination (db-RDA) revealed the presence of any of the three common helminths to be associated with significant changes in whole-gut bacterial communities (table 2 and figure 2), although the effect size was low. Instead, Syphacia spp. are associated with a gut microbiota that is divergent, in terms of composition, to that associated with H. polygyrus (figure 2). By contrast, the community composition associated with Hymenolepis spp. was not associated with either of the other two common helminths, and these differences were consistent regardless of which distance index was used (figure 2). The variance, however, explained in the helminth-associated community composition was very low (adjusted R2 ranged between 0.004 and 0.016; table 2). Helminth abundance was also associated with significant changes in the overall microbiota composition, except for Hymenolepis spp. which was marginally non-significant (p = 0.079), although, again, the proportion of variance explained was still low (adjusted R2 ranged between 0.002 and 0.014; table 2)Table 2.

Bottom Line: 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).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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biodiversity and Molecular Ecology, Centre for Research and Innovation, Fondazione Edmund Mach, Via E. Mach 1, 38010 S. Michele all'Adige, TN, Italy.

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.

No MeSH data available.


Related in: MedlinePlus