Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts

The human gut harbors numerous viruses infecting the human host, microbes, and other inhabitants of the gastrointestinal tract. Most of these viruses remain undiscovered, and their influence on human health is unknown. Here, we characterize viral genomes in gut metagenomic data from 1950 individuals...

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Main Authors: Anastasia Gulyaeva, Sanzhima Garmaeva, Alexander Kurilshikov, Arnau Vich Vila, Niels P. Riksen, Mihai G. Netea, Rinse K. Weersma, Jingyuan Fu, Alexandra Zhernakova
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Viruses
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Online Access:https://www.mdpi.com/1999-4915/14/10/2305
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author Anastasia Gulyaeva
Sanzhima Garmaeva
Alexander Kurilshikov
Arnau Vich Vila
Niels P. Riksen
Mihai G. Netea
Rinse K. Weersma
Jingyuan Fu
Alexandra Zhernakova
author_facet Anastasia Gulyaeva
Sanzhima Garmaeva
Alexander Kurilshikov
Arnau Vich Vila
Niels P. Riksen
Mihai G. Netea
Rinse K. Weersma
Jingyuan Fu
Alexandra Zhernakova
author_sort Anastasia Gulyaeva
collection DOAJ
description The human gut harbors numerous viruses infecting the human host, microbes, and other inhabitants of the gastrointestinal tract. Most of these viruses remain undiscovered, and their influence on human health is unknown. Here, we characterize viral genomes in gut metagenomic data from 1950 individuals from four population and patient cohorts. We focus on a subset of viruses that is highly abundant in the gut, remains largely uncharacterized, and allows confident complete genome identification—phages that belong to the class <i>Caudoviricetes</i> and possess genome terminal repeats. We detect 1899 species-level units belonging to this subset, 19% of which do not have complete representative genomes in major public gut virome databases. These units display diverse genomic features, are predicted to infect a wide range of microbial hosts, and on average account for <1% of metagenomic reads. Analysis of longitudinal data from 338 individuals shows that the composition of this fraction of the virome remained relatively stable over a period of 4 years. We also demonstrate that 54 species-level units are highly prevalent (detected in >5% of individuals in a cohort). Finally, we find 34 associations between highly prevalent phages and human phenotypes, 24 of which can be explained by the relative abundance of potential hosts.
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spelling doaj.art-371e61bccdf54e19baa29a652b6e8f072023-11-24T03:11:09ZengMDPI AGViruses1999-49152022-10-011410230510.3390/v14102305Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch CohortsAnastasia Gulyaeva0Sanzhima Garmaeva1Alexander Kurilshikov2Arnau Vich Vila3Niels P. Riksen4Mihai G. Netea5Rinse K. Weersma6Jingyuan Fu7Alexandra Zhernakova8Department of Genetics, University of Groningen, University Medical Center Groningen, 9713GZ Groningen, The NetherlandsDepartment of Genetics, University of Groningen, University Medical Center Groningen, 9713GZ Groningen, The NetherlandsDepartment of Genetics, University of Groningen, University Medical Center Groningen, 9713GZ Groningen, The NetherlandsDepartment of Genetics, University of Groningen, University Medical Center Groningen, 9713GZ Groningen, The NetherlandsDepartment of Internal Medicine, Radboud University Medical Center, 6525GA Nijmegen, The NetherlandsDepartment of Internal Medicine, Radboud University Medical Center, 6525GA Nijmegen, The NetherlandsDepartment of Genetics, University of Groningen, University Medical Center Groningen, 9713GZ Groningen, The NetherlandsDepartment of Genetics, University of Groningen, University Medical Center Groningen, 9713GZ Groningen, The NetherlandsDepartment of Genetics, University of Groningen, University Medical Center Groningen, 9713GZ Groningen, The NetherlandsThe human gut harbors numerous viruses infecting the human host, microbes, and other inhabitants of the gastrointestinal tract. Most of these viruses remain undiscovered, and their influence on human health is unknown. Here, we characterize viral genomes in gut metagenomic data from 1950 individuals from four population and patient cohorts. We focus on a subset of viruses that is highly abundant in the gut, remains largely uncharacterized, and allows confident complete genome identification—phages that belong to the class <i>Caudoviricetes</i> and possess genome terminal repeats. We detect 1899 species-level units belonging to this subset, 19% of which do not have complete representative genomes in major public gut virome databases. These units display diverse genomic features, are predicted to infect a wide range of microbial hosts, and on average account for <1% of metagenomic reads. Analysis of longitudinal data from 338 individuals shows that the composition of this fraction of the virome remained relatively stable over a period of 4 years. We also demonstrate that 54 species-level units are highly prevalent (detected in >5% of individuals in a cohort). Finally, we find 34 associations between highly prevalent phages and human phenotypes, 24 of which can be explained by the relative abundance of potential hosts.https://www.mdpi.com/1999-4915/14/10/2305human gut metagenome<i>Caudoviricetes</i>human phenotypes
spellingShingle Anastasia Gulyaeva
Sanzhima Garmaeva
Alexander Kurilshikov
Arnau Vich Vila
Niels P. Riksen
Mihai G. Netea
Rinse K. Weersma
Jingyuan Fu
Alexandra Zhernakova
Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts
Viruses
human gut metagenome
<i>Caudoviricetes</i>
human phenotypes
title Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts
title_full Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts
title_fullStr Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts
title_full_unstemmed Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts
title_short Diversity and Ecology of <i>Caudoviricetes</i> Phages with Genome Terminal Repeats in Fecal Metagenomes from Four Dutch Cohorts
title_sort diversity and ecology of i caudoviricetes i phages with genome terminal repeats in fecal metagenomes from four dutch cohorts
topic human gut metagenome
<i>Caudoviricetes</i>
human phenotypes
url https://www.mdpi.com/1999-4915/14/10/2305
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