|WU, S. - University Of California|
|LI, W - University Of California|
Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/9/2012
Publication Date: 5/17/2012
Citation: Wu, S., Li, R.W., Li, W., Beshah, E., Dawson, H., Uban, J.P. 2012. Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS One. 10.1371/journal.pone.0035470.
Interpretive Summary: Worm parasites (Helminths) colonize >1/3 of the world’s population and have evolved with humans and their microbiome. They are also a major problem in livestock where controlling the intensity and severity of infections are quite costly in livestock production systems. Parasites ensure survival in the host through mechanisms that dampen host inflammation. These unique properties of worms have been exploited therapeutically to treat several human diseases including inflammatory bowel diseases like Crohn's and ulcerative colitis. In order to understand the complex relations between the host, its intestinal microbiota, and the parasitic worm we characterized the pig colon microbiota in response to a parasitic infection using whole genome shotgun (WGS) and the 16S rRNA gene analysis. A significant reduction in the abundance of Fibrobacter and Ruminococcus bacteria indicated a change in the fibrolytic capacity of the colon microbiota in Trichuris suis (whipworm) infected pigs. In addition, several different biosynthetic pathways were affected that altered the metabolism in the colon of the pig. In addition, whipworm infection modulated host immunity to Campylobacter species, which can also cause disease in humans, 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 work demonstrates that parasitic worm-induced alterations in the gut microbiota may have important physiological and pathological consequences, but can also be therapeutic under certain circumstances. Understanding the interaction of these components will provide important information to enhance the health and productivity of humans and livestock.
Technical 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 ipopolysaccharide 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 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.