Abstract

Helminth infections and nutrition can independently alter the composition and abundance of the gastrointestinal microbiota, however, their combined effect is poorly understood. Here, we used the T. retortaeformis-rabbit system to examine how the helminth infection and host restriction from coprophagy/ready-to-absorb nutrients affected the duodenal microbiota, and how these changes related to the acquired immune response at the site of infection. A factorial experiment was performed where the bacterial community, its functionality and the immune response were examined in four treatments (Infect, Infect+Collar, Control+Collar and Control). Helminths reduced the diversity and abundance of the microbiota while the combination of parasites and coprophagic restriction led to a more diversified and abundant microbiota than infected cases, without significantly affecting the intensity of infection. Animals restricted from coprophagy and free from parasites exhibited the richest and most abundant bacterial community. By forcing the individuals to absorb nutrients from less digested food, the coprophagic restriction appears to have facilitated the diversity and proliferation of bacteria in the duodenum. Changes in the microbiota were more clearly associated with changes in the immune response for the infected than the nutrient restricted animals. The functional and metabolic characteristics of the duodenal microbiota were not significantly different between treatments. Overall, infection and diet affect the gut microbiota but their interactions and outcome can be complex. These findings can have important implications for the development of control measures to helminth infections where poor nutrition/malnutrition can also be a concern.

Highlights

  • The commensal microbiota of the gastrointestinal tract is a dynamic ecosystem that has to adjust to the repeated disturbance exerted by external factors while maintaining the homeostasis and functionality of the individual [1,2,3,4]

  • Given that approximately a quarter of the world population is infected with soil-transmitted helminths [16] that cause persistent, often subclinical disease and no life-long immune protection, and considering that parasites can impact host metabolism and nutrient absorption [17, 18], understanding the interaction between helminths and the gut microbiota is essential for developing new preventive approaches that can promote gastrointestinal health and overall nutrition

  • Bacteroides are more effective in stimulating the production of mucosa secretory IgA than Lactobacilli [38], and different species of Lactobacilli can regulate dendritic cells (DC) or activate natural killer (NK) cells [39]

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Summary

Introduction

The commensal microbiota of the gastrointestinal tract is a dynamic ecosystem that has to adjust to the repeated disturbance exerted by external factors while maintaining the homeostasis and functionality of the individual [1,2,3,4]. Bacteroides are more effective in stimulating the production of mucosa secretory IgA than Lactobacilli [38], and different species of Lactobacilli can regulate dendritic cells (DC) or activate natural killer (NK) cells [39] Despite these emerging properties, the relationship between the gastrointestinal microbiota and the local immune response during helminth infections is fundamentally unknown (but see [40]). Our hypothesis was that rabbits with helminths carried an impoverished bacterial community, and nutritional restrictions, by cecotrophic prevention, were expected to exacerbate this trend We anticipated both positive and negative changes in some of the components of the immune response and microbiota functionality proportional to the intensity of infection and the impact of nutritional restrictions, for example, an increase of a type 2 immune reaction in animals with parasites and restricted nutrition. This host-helminth system has many similarities with parasite infections of human and livestock and can provide fundamental knowledge on the interactions between parasitic and commensal species, their changes over the course of the infection and their association with the local immune response

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