Rodent Gut Bacteria Coexisting with an Insect Gut Virus in Parasitic Cysts: Metagenomic Evidence of Microbial Translocation and Co-adaptation in Spatially-Confined Niches

Abstract

AbstractIn medicine, parasitic cysts or cysticerci (fluid-filled cysts, larval stage of tapeworms) are believed to be sterile (no bacteria), and therein, the treatment of cysticerci infestations of deep extra-intestinal tissues (e.g., brain) relies almost exclusively on the use of antiparasitic medications, and rarely antibiotics. To date, however, it is unclear why common post-treatment complications include abscessation. This study quantified the microbial composition of parasitic cyst contents in a higher-order rodent host, using multi-kingdom shotgun metagenomics, to improve our understanding of gut microbial translocation and adaptation strategies in wild environments. Analysis was conducted on DNA from two hepatic parasitic cysts (Hydatigera (Taeenia) taeniaeformis) in an adult vole mouse (Microtus arvalis), and from feces, liver, and peritoneal fluid of three other vole family members living in a vegetable garden in Ohio, USA. Bacterial metagenomics revealed the presence of gut commensal/opportunistic species, includingParabacteroides distasonis, Klebsiella variicola, Enterococcus faecium, andLactobacillus acidophilus, inhabiting the cysts.Parabacteroides distasonisand other species were also present outside the cyst in the peritoneal fluid. Remarkably, viral metagenomics revealed various murine viral species, but unexpectedly, it detected an insect-origin virus from the army moth (Pseudaletia/Mythimna unipuncta) known as Mythimna unipuncta granulovirus A (MyunGV-A) in both cysts, and in one fecal and one peritoneal sample from two different voles, indicating survival of the insect virus and adaption in voles. Metagenomics also revealed a significantly lower probability of fungal detection in the cysts compared to other samples (peritoneal fluid, p<0.05; and feces p<0.05), with single taxon detection in each cyst forMalasseziaandPseudophaeomoniella oleicola. The samples with a higher probability of fungi were the peritoneal fluid. In conclusion, commensal/pathobiont bacterial species can inhabit parasitic tapeworm cysts, which needs to be considered during therapeutic decisions of cysticerci or other chronic disease scenarios where immune privileged and spatially restricted ecosystems with limited nutrients and minimal presence of immune cells could facilitate microbial adaptation, such as within gut wall cavitating micropathologies in Crohn’s disease.