Adult Ascaris suum roundworms and their antigens modulate the porcine intestinal microbiome and metabolome.

The porcine roundworm, Ascaris suum, affects host intestinal physiology, microbiota composition and metabolic profiles. To better understand the mediators of these alterations, six pigs each were experimentally exposed to (i) 30 adult roundworms via gastric tube, or (ii) received injections into the duodenum of A. suum total excretory-secretory (ES) antigens, ES antigens secreted exclusively from the parasites' body surface (trans-cuticular ES), or cuticular somatic antigens, respectively. Six further pigs served as untreated controls. Microbiome composition in faeces, ingesta and mucosa samples from different intestinal compartments three days after transfer was studied by next-generation 16S rDNA sequencing. Metabolite profiles were assessed in ingesta and serum samples by nuclear magnetic resonance. Transfer of adult worms and their antigens significantly affected the caecal and colonic microbiome. Adult worm transfer also led to significantly increased levels of short-chain fatty acids (SCFAs) in the colon. Similarities between pigs exposed to adult A. suum and their antigens included increased relative abundance of operational taxonomic units (OTUs) representing potentially beneficial bacteria like Lactobacillus spp., Prevotella spp., and Eubacterium coprostanoligenes, while some opportunistic pathogens like Citrobacter spp. and Mucispirillum schaedleri were also increased. The net health effect during natural A. suum infections requires further study, but these preliminary findings warrant the hypothesis that low A. suum burdens might promote intestinal health. The results further indicate that certain microbial alterations are indeed mediated by A. suum antigens, although SCFA levels were unaffected in the antigen-treated groups, possibly due to the single application. Further investigations on chronically exposed animals are warranted, especially as porcine A. suum infections serve as a model for human ascariosis.