Viral biogeography of the mammalian gut and parenchymal organs

Andrey N Shkoporov; Stephen R Stockdale; Aonghus Lavelle; Ivanela Kondova; Cara Heuston; Aditya Upadrasta; Ekaterina V Khokhlova; Imme van der Kamp; Boudewijn Ouwerling; Lorraine A Draper; Jan A M Langermans; R Paul Ross; Colin Hill

doi:10.1038/s41564-022-01178-w

Viral biogeography of the mammalian gut and parenchymal organs

Andrey N Shkoporov^*, Stephen R Stockdale, Aonghus Lavelle, Ivanela Kondova, Cara Heuston, Aditya Upadrasta, Ekaterina V Khokhlova, Imme van der Kamp, Boudewijn Ouwerling, Lorraine A Draper, Jan A M Langermans, R Paul Ross, Colin Hill^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

The mammalian virome has been linked to health and disease but our understanding of how it is structured along the longitudinal axis of the mammalian gastrointestinal tract (GIT) and other organs is limited. Here, we report a metagenomic analysis of the prokaryotic and eukaryotic virome occupying luminal and mucosa-associated habitats along the GIT, as well as parenchymal organs (liver, lung and spleen), in two representative mammalian species, the domestic pig and rhesus macaque (six animals per species). Luminal samples from the large intestine of both mammals harboured the highest loads and diversity of bacteriophages (class Caudoviricetes, family Microviridae and others). Mucosal samples contained much lower viral loads but a higher proportion of eukaryotic viruses (families Astroviridae, Caliciviridae, Parvoviridae). Parenchymal organs contained bacteriophages of gut origin, in addition to some eukaryotic viruses. Overall, GIT virome composition was specific to anatomical region and host species. Upper GIT and mucosa-specific viruses were greatly under-represented in distal colon samples (a proxy for faeces). Nonetheless, certain viral and phage species were ubiquitous in all samples from the oral cavity to the distal colon. The dataset and its accompanying methodology may provide an important resource for future work investigating the biogeography of the mammalian gut virome.

Original language	English
Pages (from-to)	1301-1311
Number of pages	11
Journal	Nature Microbiology
Volume	7
Issue number	8
DOIs	https://doi.org/10.1038/s41564-022-01178-w
Publication status	Published - Aug 2022

Bibliographical note

Funding Information:
This research was conducted with the financial support of Science Foundation Ireland (SFI) under grant number SFI/12/RC/2273 (C. Hill and R.P.R.), an SFI's Spokes Programme which is co-funded under the European Regional Development Fund under grant number SFI/14/SP APC/B3032, Wellcome Trust Research Career Development Fellowship (220646/Z/20/Z0) (A.N.S.); and a research grant from Janssen Biotech, Inc. (C. Hill and R.P.R.). This research was funded in whole, or in part, by the Wellcome Trust (220646/Z/20/Z). For the purpose of open access, the authors have applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. We thank T. Haaksma (BPRC) for his technical help with animal sampling, as well as J. Fitzgerald and J. Eckenberger for the fruitful discussion of statistical methods used in the study. The schematics in Figs. – were created with BioRender.com.

Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature Limited.

Keywords

Animals
Bacteriophages/genetics
Feces
Macaca mulatta
Mammals
Metagenome
Metagenomics
Viruses/genetics

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10.1038/s41564-022-01178-w

s41564-022-01178-wFinal published version, 15.1 MBLicence: Taverne

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title = "Viral biogeography of the mammalian gut and parenchymal organs",

abstract = "The mammalian virome has been linked to health and disease but our understanding of how it is structured along the longitudinal axis of the mammalian gastrointestinal tract (GIT) and other organs is limited. Here, we report a metagenomic analysis of the prokaryotic and eukaryotic virome occupying luminal and mucosa-associated habitats along the GIT, as well as parenchymal organs (liver, lung and spleen), in two representative mammalian species, the domestic pig and rhesus macaque (six animals per species). Luminal samples from the large intestine of both mammals harboured the highest loads and diversity of bacteriophages (class Caudoviricetes, family Microviridae and others). Mucosal samples contained much lower viral loads but a higher proportion of eukaryotic viruses (families Astroviridae, Caliciviridae, Parvoviridae). Parenchymal organs contained bacteriophages of gut origin, in addition to some eukaryotic viruses. Overall, GIT virome composition was specific to anatomical region and host species. Upper GIT and mucosa-specific viruses were greatly under-represented in distal colon samples (a proxy for faeces). Nonetheless, certain viral and phage species were ubiquitous in all samples from the oral cavity to the distal colon. The dataset and its accompanying methodology may provide an important resource for future work investigating the biogeography of the mammalian gut virome.",

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author = "Shkoporov, {Andrey N} and Stockdale, {Stephen R} and Aonghus Lavelle and Ivanela Kondova and Cara Heuston and Aditya Upadrasta and Khokhlova, {Ekaterina V} and {van der Kamp}, Imme and Boudewijn Ouwerling and Draper, {Lorraine A} and Langermans, {Jan A M} and {Paul Ross}, R and Colin Hill",

note = "Funding Information: This research was conducted with the financial support of Science Foundation Ireland (SFI) under grant number SFI/12/RC/2273 (C. Hill and R.P.R.), an SFI's Spokes Programme which is co-funded under the European Regional Development Fund under grant number SFI/14/SP APC/B3032, Wellcome Trust Research Career Development Fellowship (220646/Z/20/Z0) (A.N.S.); and a research grant from Janssen Biotech, Inc. (C. Hill and R.P.R.). This research was funded in whole, or in part, by the Wellcome Trust (220646/Z/20/Z). For the purpose of open access, the authors have applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. We thank T. Haaksma (BPRC) for his technical help with animal sampling, as well as J. Fitzgerald and J. Eckenberger for the fruitful discussion of statistical methods used in the study. The schematics in Figs. – were created with BioRender.com. Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature Limited.",

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doi = "10.1038/s41564-022-01178-w",

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AU - Shkoporov, Andrey N

AU - Stockdale, Stephen R

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AU - Kondova, Ivanela

AU - Heuston, Cara

AU - Upadrasta, Aditya

AU - Khokhlova, Ekaterina V

AU - van der Kamp, Imme

AU - Ouwerling, Boudewijn

AU - Draper, Lorraine A

AU - Langermans, Jan A M

AU - Paul Ross, R

AU - Hill, Colin

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Viral biogeography of the mammalian gut and parenchymal organs

Abstract

Bibliographical note

Keywords

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