Rodent Gut Bacteria Coexisting with an Insect Gut Virus in Tapeworm Parasitic Cysts: Metagenomic Evidence of Microbial Selection in Extra-Intestinal Clinical Niches

Author:

Ammar Amro12,Singh Vaidhvi12,Ilic Sanja3ORCID,Samiksha Fnu4,Marsh Antoinette5,Rodriguez-Palacios Alexander1267ORCID

Affiliation:

1. Division of Gastroenterology and Liver Disease, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA

2. Digestive Health Research Institute, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA

3. Department of Human Sciences, Human Nutrition and Food Microbiology, The Ohio State University, Columbus, OH 43210, USA

4. Department of Cancer Biology, Learner Research Institute, Cleveland Clinic, Cleveland, OH 44106, USA

5. The Veterinary Medical Center Diagnostic Parasitology, Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210, USA

6. Department of Molecular Biology and Microbiology, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA

7. University Hospitals Research and Education Institute, University Hospitals Cleveland Medical Center, Cleveland, OH 44106, USA

Abstract

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.

Funder

NIH

Publisher

MDPI AG

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