Metabolic arsenal of giant viruses: Host hijack or self-use?

Belhaouari, Djamal Brahim; Pires, Gabriel Augusto; Lamb, David; Kelly, Steven; Goldstone, Jared V; Stegeman, John J; Colson, Philippe; Scola, Bernard La; Aherfi, Sarah

doi:10.7554/elife.78674

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Metabolic arsenal of giant viruses: Host hijack or self-use?

Djamal Brahim Belhaouari, Gabriel Augusto Pires De Souza, David Lamb

, Steven Kelly

, Jared V Goldstone, John J Stegeman

, Philippe Colson, Bernard La Scola, Sarah Aherfi

eLife, Volume: 11

Swansea University Authors: David Lamb , Steven Kelly

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DOI (Published version): 10.7554/elife.78674

Abstract

Viruses generally are defined as lacking the fundamental properties of living organisms in that they do not harbor an energy metabolism system or protein synthesis machinery. However, the discovery of giant viruses of amoeba has fundamentally challenged this view because of their exceptional genome...

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Published in:	eLife
ISSN:	2050-084X
Published:	eLife Sciences Publications, Ltd 2022
Online Access:	Check full text
URI:	https://cronfa.swan.ac.uk/Record/cronfa60435
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first_indexed	2022-07-12T13:06:25Z
last_indexed	2023-01-13T19:20:33Z
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spelling	2022-07-12T14:08:07.1372153 v2 60435 2022-07-11 Metabolic arsenal of giant viruses: Host hijack or self-use? 1dc64e55c2c28d107ef7c3db984cccd2 0000-0001-5446-2997 David Lamb David Lamb true false b17cebaf09b4d737b9378a3581e3de93 0000-0001-7991-5040 Steven Kelly Steven Kelly true false 2022-07-11 BMS Viruses generally are defined as lacking the fundamental properties of living organisms in that they do not harbor an energy metabolism system or protein synthesis machinery. However, the discovery of giant viruses of amoeba has fundamentally challenged this view because of their exceptional genome properties, particle sizes and encoding of the enzyme machinery for some steps of protein synthesis. Although giant viruses are not able to replicate autonomously and still require a host for their multiplication, numerous metabolic genes involved in energy production have been recently detected in giant virus genomes from many environments. These findings have further blurred the boundaries that separate viruses and living organisms. Herein, we summarize information concerning genes and proteins involved in cellular metabolic pathways and their orthologues that have, surprisingly, been discovered in giant viruses. The remarkable diversity of metabolic genes described in giant viruses include genes encoding enzymes involved in glycolysis, gluconeogenesis, tricarboxylic acid cycle, photosynthesis, and β-oxidation. These viral genes are thought to have been acquired from diverse biological sources through lateral gene transfer early in the evolution of Nucleo-Cytoplasmic Large DNA Viruses, or in some cases more recently. It was assumed that viruses are capable of hijacking host metabolic networks. But the giant virus auxiliary metabolic genes also may represent another form of host metabolism manipulation, by expanding the catalytic capabilities of the host cells especially in harsh environments, providing the infected host cells with a selective evolutionary advantage compared to non-infected cells and hence favoring the viral replication. However, the mechanism of these genes' functionality remains unclear to date. Journal Article eLife 11 eLife Sciences Publications, Ltd 2050-084X 8 7 2022 2022-07-08 10.7554/elife.78674 COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University Royal Society; Woods Hole Center for Oceans and Human Health; National Institutes of Health (P01ES021923); National Science Foundation (OCE-1314642); Agence Nationale de la Recherche ("Investments for the Future" program Méditerranée-Infection 10-IAHU-03). 2022-07-12T14:08:07.1372153 2022-07-11T08:31:30.8245303 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Djamal Brahim Belhaouari 1 Gabriel Augusto Pires De Souza 2 David Lamb 0000-0001-5446-2997 3 Steven Kelly 0000-0001-7991-5040 4 Jared V Goldstone 5 John J Stegeman 0000-0001-8204-5357 6 Philippe Colson 7 Bernard La Scola 8 Sarah Aherfi 0000-0002-5253-1757 9 60435__24553__ac28abf2ef724581adfc9b093087895a.pdf 60435_VoR.pdf 2022-07-12T14:06:48.8504448 Output 1826998 application/pdf Version of Record true Copyright Brahim Belhaouari et al. This article is distributed under the terms of the Creative Commons Attribution License true eng http://creativecommons.org/licenses/by/4.0/
title	Metabolic arsenal of giant viruses: Host hijack or self-use?
spellingShingle	Metabolic arsenal of giant viruses: Host hijack or self-use? David Lamb Steven Kelly
title_short	Metabolic arsenal of giant viruses: Host hijack or self-use?
title_full	Metabolic arsenal of giant viruses: Host hijack or self-use?
title_fullStr	Metabolic arsenal of giant viruses: Host hijack or self-use?
title_full_unstemmed	Metabolic arsenal of giant viruses: Host hijack or self-use?
title_sort	Metabolic arsenal of giant viruses: Host hijack or self-use?
author_id_str_mv	1dc64e55c2c28d107ef7c3db984cccd2 b17cebaf09b4d737b9378a3581e3de93
author_id_fullname_str_mv	1dc64e55c2c28d107ef7c3db984cccd2_*_David Lamb b17cebaf09b4d737b9378a3581e3de93_*_Steven Kelly
author	David Lamb Steven Kelly
author2	Djamal Brahim Belhaouari Gabriel Augusto Pires De Souza David Lamb Steven Kelly Jared V Goldstone John J Stegeman Philippe Colson Bernard La Scola Sarah Aherfi
format	Journal article
container_title	eLife
container_volume	11
publishDate	2022
institution	Swansea University
issn	2050-084X
doi_str_mv	10.7554/elife.78674
publisher	eLife Sciences Publications, Ltd
college_str	Faculty of Medicine, Health and Life Sciences
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hierarchy_top_title	Faculty of Medicine, Health and Life Sciences
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department_str	Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
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description	Viruses generally are defined as lacking the fundamental properties of living organisms in that they do not harbor an energy metabolism system or protein synthesis machinery. However, the discovery of giant viruses of amoeba has fundamentally challenged this view because of their exceptional genome properties, particle sizes and encoding of the enzyme machinery for some steps of protein synthesis. Although giant viruses are not able to replicate autonomously and still require a host for their multiplication, numerous metabolic genes involved in energy production have been recently detected in giant virus genomes from many environments. These findings have further blurred the boundaries that separate viruses and living organisms. Herein, we summarize information concerning genes and proteins involved in cellular metabolic pathways and their orthologues that have, surprisingly, been discovered in giant viruses. The remarkable diversity of metabolic genes described in giant viruses include genes encoding enzymes involved in glycolysis, gluconeogenesis, tricarboxylic acid cycle, photosynthesis, and β-oxidation. These viral genes are thought to have been acquired from diverse biological sources through lateral gene transfer early in the evolution of Nucleo-Cytoplasmic Large DNA Viruses, or in some cases more recently. It was assumed that viruses are capable of hijacking host metabolic networks. But the giant virus auxiliary metabolic genes also may represent another form of host metabolism manipulation, by expanding the catalytic capabilities of the host cells especially in harsh environments, providing the infected host cells with a selective evolutionary advantage compared to non-infected cells and hence favoring the viral replication. However, the mechanism of these genes' functionality remains unclear to date.
published_date	2022-07-08T04:18:32Z
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score	11.017776

Metabolic arsenal of giant viruses: Host hijack or self-use?

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