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Title: Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection

Author
item WU, SITAO - University Of California
item Li, Robert
item LI, WEIZHONG - University Of California
item Urban, Joseph
item Dawson, Harry
item Beshah, Ethiopia

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/16/2012
Publication Date: 4/20/2012
Citation: Wu, S., Li, R.W., Li, W., Urban Jr, J.F., Dawson, H.D., Beshah, E. 2012. Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS One. 7(4):e35470.

Interpretive Summary: A parasitic nematode called the whipworm negatively influences animal meat production around the world. This parasite is known to be effective in treating human disease via its role in rebalancing the immune systems. Pigs infected with the whipworm showed profound changes in the microbial composition in the proximal colon and had a significant reduction in fiber-utilizing capacity in the gut. Our results provide insight into the dynamics of the gut microbial ecosystem and will guide our effort to formulate optimal diets to ameliorate symptoms resulting from infection in pigs as well as to reduce possible side effects during human therapy. Pig farmers will directly benefit from our study by having diets formulated to ameliorate symptoms and reduce pathology from parasitic infection. Furthermore, patients with autoimmune diseases, such as Crohn’s disease and ulcerative colitis, could benefit from this study by having a safe and efficacious helminth therapy.

Technical Abstract: The similar biology of several helminth infections in pigs and humans provides an excellent animal model to study the interaction between the host and parasite infection that could have important consequences for human health. We had observed that pigs infected with the whipworm Trichuris suis for 21 days showed profound changes in the proximal colon microbiota. In this follow-up study, changes in the microbial composition and metabolic potentials in the proximal colon microbiota of parasite naïve pigs and infected pigs that maintained adult T. suis worms or expelled the worms from the colon were investigated using metagenomic tools. Pigs were inoculated with a single dose of T. suis eggs and evaluated 53 days later; age-matched uninfected pigs served as parasite naïve controls. Among infected pigs, two cohorts were differentiated that either had adult worms or were worm-free. Infection resulted in a significant change in the relative abundance of approximately 13% of genera detected in the porcine proximal colon microbiota regardless of worm status suggesting a relatively persistent change in the microbiota due to infection over time. A notable change in the fibrolytic capacity of the proximal colon microbiota was observed in T. suis infected pigs evidenced by a significant reduction in the relative abundance of Fibrobacter and Ruminococcus. In addition, ~ 10% of identified KEGG pathways were affected by infection, including ABC transporters, peptidoglycan biosynthesis, and lipopolysaccharide biosynthesis as well as a-linolenic acid metabolism. Trichuris suis infection modulated host immunity to Campylobacter because there was a 3-fold increase in the relative abundance in the proximal colon microbiota of infected pigs with worms compared to uninfected controls, but a 3-fold reduction in worm-free infected pigs compared to controls. Our findings provided insight into the dynamics of the proximal colon microbiota in pigs in response to T. suis infection that can be either inflammatory or therapeutic.