RESUMO
In medicine, parasitic cysts (e.g., brain cysticerci) are believed to be sterile, and are primarily treated with antiparasitic medications, not antibiotics, which could prevent abscess formation and localized inflammation. This study quantified the microbial composition of parasitic cysts in a wild rodent, using multi-kingdom metagenomics to comprehensively assess if parasitic cysts are sterile, and further understand gut microbial translocation and adaptation in wildlife confined environments, outside the gut. Analysis was conducted on DNA from two hepatic parasitic cysts from a feline tapeworm, Hydatigera (Taenia) taeniaeformis, affecting a wild vole mouse (Microtus pennsylvanicus), and from feces, liver and peritoneal fluid of this and two other concurrent individual wild voles trapped during pest control in one of our university research vegetable gardens. Bacterial metagenomics revealed the presence of gut commensal/opportunistic species, Parabacteroides distasonis, Bacteroides (Bacteroidota); Klebsiella variicola, E. coli (Enterobacteriaceae); Enterococcus faecium and Lactobacillus acidophilus (Bacillota) inhabiting the cysts, and peritoneal fluid. Remarkably, viral metagenomics revealed various murine viral species, and unexpectedly, a virus from the insect armyworm moth (Pseudaletia/Mythimna unipuncta), known as Mythimna unipuncta granulovirus A (MyunGV-A), in both cysts, and in one fecal and one peritoneal sample from the other non-cyst voles, indicating the survival and adaption potential of the insect virus in voles. Metagenomics also revealed a significantly lower probability of fungal detection in cysts compared to that in peritoneal fluid/feces (p < 0.05), with single taxon detection in each cyst (Malassezia and Pseudophaeomoniella oleicola). The peritoneal fluid had the highest probability for fungi. In conclusion, metagenomics revealed that bacteria/viruses/fungi coexist within parasitic cysts supporting the potential therapeutic benefits of antibiotics in cystic diseases, and in inflammatory microniches of chronic diseases, such as Crohn's disease gut wall cavitating micropathologies, from which we recently isolated similar synergistic pathogenic Bacteroidota and Enterobacteriaceae, and Bacillota.
RESUMO
In 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, including Parabacteroides distasonis, Klebsiella variicola, Enterococcus faecium, and Lactobacillus acidophilus, inhabiting the cysts. Parabacteroides distasonis and 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 for Malassezia and Pseudophaeomoniella 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.