A Previously Undescribed Highly Prevalent Phage Identified in a Danish Enteric Virome Catalog

Lore Van Espen, Emilie Glad Bak, Leen Beller, Lila Close, Ward Deboutte, Helene Bæk Juel, Trine Nielsen, Deniz Sinar, Lander De Coninck, Christine Frithioff-Bøjsøe, Cilius Esmann Fonvig, Suganya Jacobsen, Maria Kjærgaard, Maja Thiele, Anthony Fullam, Michael Kuhn, Jens Christian Holm, Peer Bork, Aleksander Krag, Torben HansenManimozhiyan Arumugam, Jelle Matthijnssens*

*Kontaktforfatter for dette arbejde

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Abstrakt

Gut viruses are important, yet often neglected, players in the complex human gut microbial ecosystem. Recently, the number of human gut virome studies has been increasing; however, we are still only scratching the surface of the immense viral diversity. In this study, 254 virus-enriched fecal metagenomes from 204 Danish subjects were used to generate the Danish Enteric Vir ome Catalog (DEVoC) containing 12,986 nonredundant viral scaffolds, of which the majority was previously undescribed, encoding 190,029 viral genes. The DEVoC was used to compare 91 healthy DEVoC gut viromes from children, adolescents, and adults that were used to create the DEVoC. Gut viromes of healthy Danish subjects were dominated by phages. While most phage genomes (PGs) only occurred in a single subject, indicating large virome individuality, 39 PGs were present in more than 10 healthy subjects. Among these 39 PGs, the prevalences of three PGs were associated with age. To further study the prevalence of these 39 prevalent PGs, 1,880 gut virome data sets of 27 studies from across the world were screened, revealing several age-, geography-, and disease-related prevalence patterns. Two PGs also showed a remarkably high prevalence worldwide-a crAss-like phage (20.6% prevalence), belonging to the tentative AlphacrAssvirinae subfamily, and a previously undescribed circular temperate phage infecting Bacteroides dorei (14.4% prevalence), called LoVEphage because it encodes lots of viral elements. Due to the LoVEphage's high prevalence and novelty, public data sets in which the LoVEphage was detected were de novo assembled, resulting in an additional 18 circular LoVEphage-like genomes (67.9 to 72.4 kb). IMPORTANCE Through generation of the DEVoC, we added numerous previously uncharacterized viral genomes and genes to the ever-increasing worldwide pool of human gut viromes. The DEVoC, the largest human gut virome catalog generated from consistently processed fecal samples, facilitated the analysis of the 91 healthy Danish gut viromes. Characterizing the biggest cohort of healthy gut viromes from children, adolescents, and adults to date confirmed the previously established high interindividual variation in human gut viromes and demonstrated that the effect of age on the gut virome composition was limited to the prevalence of specific phage (groups). The identification of a previously undescribed prevalent phage illustrates the usefulness of developing virome catalogs, and we foresee that the DEVoC will benefit future analysis of the roles of gut viruses in human health and disease.

OriginalsprogEngelsk
Artikelnummere00382-21
TidsskriftmSystems
Vol/bind6
Udgave nummer5
DOI
StatusUdgivet - sep. 2021

Bibliografisk note

Funding Information:
This research was supported by the Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark (grant number NNF18CC0034900), the Challenge Grant “MicrobLiver” (grant number NNF15OC0016692), and grant number NNF15OC0016544 from the Novo Nordisk Foundation; the Innovation Fund Denmark (TARGET: grant number 0603-00484B), the Region Zealand Health Scientific Research Foundation; and the European Union’s Horizon 2020 research and innovation program (GALAXY: grant number 668031); the “Fonds Wetenschappelijk Onderzoek” (FWO, Research Foundation Flanders) (Lore Van Espen: 1S25720N, Leen Beller: 1S61618N).

Funding Information:
This research was supported by the Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark (grant number NNF18CC0034900), the Challenge Grant "MicrobLiver" (grant number NNF15OC0016692), and grant number NNF15OC0016544 from the Novo Nordisk Foundation; the Innovation Fund Denmark (TARGET: grant number 0603- 00484B), the Region Zealand Health Scientific Research Foundation; and the European Union's Horizon 2020 research and innovation program (GALAXY: grant number 668031); the "Fonds Wetenschappelijk Onderzoek" (FWO, Research Foundation Flanders) (Lore Van Espen: 1S25720N, Leen Beller: 1S61618N).

Funding Information:
The computational resources were provided by the Flemish Supercomputer Center (VSC) and funded by FWO and the Flemish Government Department of Economy, Science, and Innovation.

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