Abstract
Helminth infection in pigs serves as an excellent model for the study of the interaction between human malnutrition and parasitic infection and could have important implications in human health. We had observed that pigs infected with Trichuris suis for 21 days showed significant changes in the proximal colon microbiota. In this study, interactions between worm burden and severity of disruptions to the microbial composition and metabolic potentials in the porcine proximal colon microbiota were investigated using metagenomic tools. Pigs were infected by a single dose of T. suis eggs for 53 days. Among infected pigs, two cohorts were differentiated that either had adult worms or were worm-free. Infection resulted in a significant change in the abundance of approximately 13% of genera detected in the proximal colon microbiota regardless of worm status, suggesting a relatively persistent change over time in the microbiota due to the initial infection. A significant reduction in the abundance of Fibrobacter and Ruminococcus indicated a change in the fibrolytic capacity of the colon microbiota in T. suis infected pigs. In addition, ∼10% of identified KEGG pathways were affected by infection, including ABC transporters, peptidoglycan biosynthesis, and lipopolysaccharide biosynthesis as well as α-linolenic acid metabolism. Trichuris suis infection modulated host immunity to Campylobacter because there was a 3-fold increase in the relative abundance in the colon microbiota of infected pigs with worms compared to naïve controls, but a 3-fold reduction in worm-free infected pigs compared to controls. The level of pathology observed in infected pigs with worms compared to worm-free infected pigs may relate to the local host response because expression of several Th2-related genes were enhanced in infected pigs with worms versus those worm-free. Our findings provided insight into the dynamics of the proximal colon microbiota in pigs in response to T. suis infection.
Highlights
Swine have been widely used as a model for human diseases due to anatomic, physiological, and immunological similarities between the two species [1]
The whipworm Trichuris suis in pigs is an example of a common helminth infection that results in generally mild symptoms, such as diarrhea, anorexia, and retarded growth commonly controlled by management and anthelmintic drugs, but is a re-emerging problem especially in organic and free-range pig production systems
Worm burden and changes in localized inflammation The adult T. suis worm burden and associated pathology in the proximal colon become more disparate in a group of out-bred pigs between seven and nine weeks after inoculation with some pigs showing fewer than worms and an apparently normal mucosa and others showing hundreds of worms with localized inflammation, mucus production, and smooth muscle hypertrophy; worm clearance is virtually complete between weeks 9 and [15]
Summary
Swine have been widely used as a model for human diseases due to anatomic, physiological, and immunological similarities between the two species [1]. Diverse genetic resources in pigs are readily available, which frequently leads to a whole spectrum of phenotypic changes in response to infection with bacteria, viruses, and parasites common to humans as well as similar dietary patterns. Several studies have suggested that probiotics within the genera Lactobacillus and Bifidobacterium may have favorable impact on the treatment of patients with CD by altering the gut microbiota and modulating the host immune system [14]. We demonstrated that a 21-day T. suis infection in pigs induced a profound change in both microbial composition and metabolic potential in the lumen of the proximal colon [2]. We investigated the relationship between adult T. suis worm burden and changes in the pig proximal colon luminal microbiota. The results indicated that T. suis-induced changes in the proximal colon microbiota were similar regardless of the persistence or host clearance of adult worms. The local host mucosal response was associated with worm burden and the intensity of Th2-related and allergy/ asthma associated gene expression
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