Infection with the sheep gastrointestinal nematode Teladorsagia circumcincta increases luminal pathobionts

Abstract

Background: The multifaceted interactions between gastrointestinal (GI) helminth parasites, host gut microbiota and immune system are emerging as a key area of research within the field of host-parasite relationships. In spite of the plethora of data available on the impact that GI helminths exert on the composition of the gut microflora, whether alterations of microbial profiles are caused by direct parasite-bacteria interactions or, indirectly, by alterations of the GI environment (e.g. mucosal immunity) remains to be determined. Furthermore, no data is thus far available on the downstream roles that qualitative and quantitative changes in gut microbial composition play in the overall pathophysiology of parasite infection and disease. Results: In this study, we investigated the fluctuations in microbiota composition and local immune microenvironment of sheep vaccinated against, and experimentally infected with, the 'brown stomach worm' Teladorsagia circumcincta, a parasite of worldwide socioeconomic significance. We compared the faecal microbial profiles of vaccinated and subsequently infected sheep with those obtained from groups of unvaccinated/infected and unvaccinated/ uninfected animals. We show that alterations of gut microbial composition are associated mainly with parasite infection, and that this involves the expansion of populations of bacteria with known pro-inflammatory properties that may contribute to the immunopathology of helminth disease. Using novel quantitative approaches for the analysis of confocal microscopy-derived images, we also show that gastric tissue infiltration of T cells is driven by parasitic infection rather than anti-helminth vaccination. Conclusions: Teladorsagia circumcincta infection leads to an expansion of potentially pro-inflammatory gut microbial species and abomasal T cells. This data paves the way for future experiments aimed to determine the contribution of the gut flora to the pathophysiology of parasitic disease, with the ultimate aim to design and develop novel treatment/control strategies focused on preventing and/or restricting bacterial-mediated inflammation upon infection by GI helminths.

Emerging interactions between diet, gastrointestinal helminth infection, and the gut microbiota in livestock

“…In contrast to these studies, cattle that were rendered immune to O. ostertagi through serial immunisation by drug-abbreviated infections showed no changes in abomasal microbiota composition following a challenge infection [ 48 ]. This may indicate that rapid expulsion of larvae from immune animals is insufficient to drive changes in microbiota, consistent with reports that vaccine-induced Th2-polarized immune changes also do not appear to cause significant alteration of the GM in sheep [ 45 ]. However, studies in primary O. ostertagi infections with an established adult worm population have not been reported, and further work is needed to delineate the differential effects of acute and chronic infection in parasite-naïve or immune animals.…”

“…In sheep infected with both H. contortus and T. circumcincta , faecal microbiota profiles showed only minor differences over time but did indicate a progressive decrease in alpha-diversity in infected animals [ 44 ]. Cortés et al [ 45 ] have shown that in young sheep mono-infected with T. circumcincta , no change in faecal alpha-diversity was reported but significant increases in abundance of Prevotella spp. as well as the putatively pathogenic Sutterella spp.…”

The Maintenance of Microbial Community in Human Fecal Samples by a Self-made Cost-effective Preservation Buffer

“…In recent years, accumulating attentions have been paid to a long-neglected fact that samples guarantee the reliability of studies via providing stable microbiome. Given that longitudinal investigations in the current microbiota era are wellcharacterized by various subjects and a vast geographical coverage [10][11][12][13][14][15][16] , the development and utilization of preservation methods are particularly important to hold samples eligible for the consequent sequencing analysis. In the present work, we performed shotgun sequencing and demonstrated that in a short-term storage, microbial consortia in human fecal samples were substantially maintained, independent of the accompanied storage temperature.…”

“…Immediate cryopreservation at -80°C or snap freezing with liquid nitrogen (LN) is considered as the 'gold standard' of sample preservation 7,9 . However, microbiome studies in the present era have already intensively expanded in terms of geographic region and species diversity [10][11][12][13][14][15][16] , ranging from urban cities (e.g. human, laboratory organisms, companion animals) to remote areas (e.g.…”

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“…via changes to worm burdens (6) and effects on parasite immune-modulatory properties (6)(7)(8)(9). Other investigations suggest that the host gut flora contributes to the gastrointestinal pathology associated with helminth infection (10,11). Nonetheless, disentangling the immune-molecular mechanisms that underpin these interactions is essential for establishing causal relationships between helminths and the gut microbiota.…”