Abstract

Phages (viruses that infect bacteria) play important roles in the gut ecosystem through infection of bacterial hosts, yet the gut virome remains poorly characterized. Mammalian gut viromes are dominated by double-stranded DNA (dsDNA) phages belonging to the order Caudovirales and single-stranded DNA (ssDNA) phages belonging to the family Microviridae. Since the relative proportion of each of these phage groups appears to correlate with age and health status in humans, it is critical to understand both ssDNA and dsDNA phages in the gut. Building upon prior research describing dsDNA viruses in the gut of Ciona robusta, a marine invertebrate model system used to study gut microbial interactions, this study investigated ssDNA phages found in the Ciona gut. We identified 258 Microviridae genomes, which were dominated by novel members of the Gokushovirinae subfamily, but also represented several proposed phylogenetic groups (Alpavirinae, Aravirinae, Group D, Parabacteroides prophages, and Pequeñovirus) and a novel group. Comparative analyses between Ciona specimens with full and cleared guts, as well as the surrounding water, indicated that Ciona retains a distinct and highly diverse community of ssDNA phages. This study significantly expands the known diversity within the Microviridae family and demonstrates the promise of Ciona as a model system for investigating their role in animal health.

Highlights

  • Recent studies of host-microbe interactions have recognized the importance of the holobiont, which acknowledges the complex partnerships between an animal and the entirety of its associated microbial communities [1]

  • While phage dynamics likely have dramatic influences on the physiology of the animal host, very little is known about the role of viromes or their impacts within the gut environment [6,8,9,10,25,26,27,28,29,30]

  • The main objectives of the current study were to: (1) characterize the diversity of complete circular genomes related to the Microviridae, the most widely detected single-stranded DNA (ssDNA) phages among animals, from the Ciona gut, (2) evaluate if the identified ssDNA phages were unique to Ciona or if they were found in water samples, and (3) determine if different gut compartments contained distinct ssDNA

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Summary

Introduction

Recent studies of host-microbe interactions have recognized the importance of the holobiont, which acknowledges the complex partnerships between an animal and the entirety of its associated microbial communities [1]. Significant attention has been given to the metabolic contributions from the cellular component of the microbiome (i.e., bacteria, archaea, and fungi), it is recognized that viruses play important roles in the holobiont, both directly through infecting animal host cells, and indirectly through mediating microbiome dynamics. While phage dynamics likely have dramatic influences on the physiology of the animal host, very little is known about the role of viromes (the cumulative viral community associated with a given host) or their impacts within the gut environment [6,8,9,10,25,26,27,28,29,30]

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