Ascaris suum infection was associated with a worm-independent reduction in microbial diversity and altered metabolic potential in the porcine gut microbiome

Authors: WANG, YUEYING - Henan Agricultural University; LIU, FANG - Ocean University Of China; Urban, Joseph; PAEREWIJCK, OONAGH - Ghent University; GELDHOF, PETER - Ghent University; Li, Robert

Submitted to: International Journal for Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/26/2018
Publication Date: 2/8/2019
Citation: Wang, Y., Liu, F., Urban Jr, J.F., Paerewijck, O., Geldhof, P., Li, R.W. 2019. Ascaris suum infection was associated with a worm-independent reduction in microbial diversity and altered metabolic potential in the porcine gut microbiome. International Journal for Parasitology. 49(3-4):247-256. https://doi.org/10.1016/j.ijpara.2018.10.007.
DOI: https://doi.org/10.1016/j.ijpara.2018.10.007

Interpretive Summary: The roundworm Ascaris suum is a ubiquitous parasitic nematode that causes infection with high prevalence rates in swine and leads to a significant economical loss to pig farmers. It has become clear in the past few years that this parasite is zoonotic in developed countries and probably in developing countries as well. Moreover, the infection by Ascaris suum can also serve as a valuable disease model for human Ascariasis, which affects 807 million to 1.2 billion people globally. In this study, we investigated the effect of A. suum on the structure and function of the porcine intestinal microbiome. Our findings demonstrated that the infection resulted in a significant reduction in the gut microbial diversity and had a broad impact on the metabolic potential of the intestinal microbial community. Our investigation will undoubtedly expand our understanding of pathological consequences of the Ascaris infection in both humans and pigs and generate hypotheses and identify novel areas for future research.

Technical Abstract: Gastrointestinal nematode infections have a serious impact on the health of humans and animals. Previous studies demonstrate that helminth infections alter the composition and structure of intestinal microbiome while the interaction between parasites and intestinal microbiome can further influence host immunity and intestinal inflammation. In this study, the effect of Ascaris suum infection on the microbial composition in the proximal colon and fecal matters of pigs was investigated using 16S rRNA gene sequencing. Our data showed that the infection significantly decreased various microbial diversity indices, such as richness (Chao1) and evenness, as well as Phylogenetic Diversity (PD whole tree). The effect of the infection on Chao1 of the colon luminal contents is worm-burden independent. Among the 16 phyla identified, the relative abundance of the phyla Spirochaetes and Planctomycetes were significantly altered by infection. The abundance of approximately 29% of the genera present in colon contents, such as Prevotella and Faecalibacterium, and 179 operational taxonomic units (OTUs) was significantly changed by infection. Intriguingly, infection also led to a significant shift in the metabolic potential of the proximal colon microbiome, where the relative abundance of at least 58 metabolic pathways was affected, including those related to carbohydrate metabolism and amino acid metabolism. Overall, our findings indicate the Ascaris infection induced a profound change in the gut microbiome, especially at the site of infection and should facilitate our understanding of the pathophysiological consequence of gastrointestinal nematodes.