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Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?

Sarah Aherfi, Djamal Brahim Belhaouari Orcid Logo, Lucile Pinault Orcid Logo, Jean-Pierre Baudoin, Philippe Decloquement, Jonatas Abrahao, Philippe Colson, Anthony Levasseur, David Lamb Orcid Logo, Eric Chabriere, Didier Raoult Orcid Logo, Bernard La Scola Orcid Logo

The ISME Journal, Volume: 16, Issue: 3, Pages: 695 - 704

Swansea University Author: David Lamb Orcid Logo

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DOI (Published version): 10.1038/s41396-021-01117-3

Abstract

The discovery of Acanthamoeba polyphaga Mimivirus, the first isolated giant virus of amoeba, challenged the historical hallmarks defining a virus. Giant virion sizes are known to reach up to 2.3µm, making them visible by optical microscopy. Their large genome sizes of up to 2.5Mb can encode proteins...

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Published in: The ISME Journal
ISSN: 1751-7362 1751-7370
Published: Springer Nature Springer Science and Business Media LLC 2022
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URI: https://cronfa.swan.ac.uk/Record/cronfa57909
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spelling 2022-10-27T11:26:21.0312057 v2 57909 2021-09-16 Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus? 1dc64e55c2c28d107ef7c3db984cccd2 0000-0001-5446-2997 David Lamb David Lamb true false 2021-09-16 BMS The discovery of Acanthamoeba polyphaga Mimivirus, the first isolated giant virus of amoeba, challenged the historical hallmarks defining a virus. Giant virion sizes are known to reach up to 2.3µm, making them visible by optical microscopy. Their large genome sizes of up to 2.5Mb can encode proteins involved in the translation apparatus. We have investigated possible energy production in Pandoravirus massiliensis. Mitochondrial membrane markers allowed for the detection of a membrane potential in purified virions and this was enhanced by a regulator of the tricarboxylic acid cycle but abolished by the use of a depolarizing agent. Bioinformatics was employed to identify enzymes involved in virion proton gradient generation and this approach revealed that 8 putative P. massiliensis proteins exhibited low sequence identities with known cellular enzymes involved in the universal tricarboxylic acid cycle. Further, all 8 viral genes were transcribed during replication. The product of one of these genes, ORF132, was cloned and expressed in Escherichia coli, and shown to function as an isocitrate dehydrogenase, a key enzyme of the tricarboxylic acid cycle. Our findings show for the first time that a membrane potential can exist in Pandoraviruses, and this may be related to tricarboxylic acid cycle. The presence of a proton gradient in P. massiliensis makes this virus a form of life for which it is legitimate to ask the question ‘what is a virus?’. Journal Article The ISME Journal 16 3 695 704 Springer Science and Business Media LLC Springer Nature 1751-7362 1751-7370 giant viruses; Pandoravirus; energy metabolism; ATP production; Lipman 25 system; tricarboxylic acid cycle 1 3 2022 2022-03-01 10.1038/s41396-021-01117-3 COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University This work was supported by the French Government under the “Investments for the Future” program managed by the National Agency for Research (ANR), MéditerranéeInfection 10-IAHU-03. It was also supported by Région Provence-Alpes-Côte d’Azur and European funding FEDER PRIMMI (Fonds Européen de Développement Régional— Plateformes de Recherche et d’Innovation Mutualisées Méditerranée Infection). 2022-10-27T11:26:21.0312057 2021-09-16T10:50:45.8231563 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Sarah Aherfi 1 Djamal Brahim Belhaouari 0000-0002-1112-9921 2 Lucile Pinault 0000-0001-8655-6349 3 Jean-Pierre Baudoin 4 Philippe Decloquement 5 Jonatas Abrahao 6 Philippe Colson 7 Anthony Levasseur 8 David Lamb 0000-0001-5446-2997 9 Eric Chabriere 10 Didier Raoult 0000-0002-0633-5974 11 Bernard La Scola 0000-0001-8006-7704 12 57909__21043__121b5477a5ff43599c49ee2681cb8648.pdf 57909.pdf 2021-09-28T17:34:29.1414644 Output 1596014 application/pdf Version of Record true © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License true eng http://creativecommons.org/licenses/by/4.0/
title Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?
spellingShingle Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?
David Lamb
title_short Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?
title_full Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?
title_fullStr Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?
title_full_unstemmed Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?
title_sort Incomplete tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: is it still a virus?
author_id_str_mv 1dc64e55c2c28d107ef7c3db984cccd2
author_id_fullname_str_mv 1dc64e55c2c28d107ef7c3db984cccd2_***_David Lamb
author David Lamb
author2 Sarah Aherfi
Djamal Brahim Belhaouari
Lucile Pinault
Jean-Pierre Baudoin
Philippe Decloquement
Jonatas Abrahao
Philippe Colson
Anthony Levasseur
David Lamb
Eric Chabriere
Didier Raoult
Bernard La Scola
format Journal article
container_title The ISME Journal
container_volume 16
container_issue 3
container_start_page 695
publishDate 2022
institution Swansea University
issn 1751-7362
1751-7370
doi_str_mv 10.1038/s41396-021-01117-3
publisher Springer Science and Business Media LLC
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
document_store_str 1
active_str 0
description The discovery of Acanthamoeba polyphaga Mimivirus, the first isolated giant virus of amoeba, challenged the historical hallmarks defining a virus. Giant virion sizes are known to reach up to 2.3µm, making them visible by optical microscopy. Their large genome sizes of up to 2.5Mb can encode proteins involved in the translation apparatus. We have investigated possible energy production in Pandoravirus massiliensis. Mitochondrial membrane markers allowed for the detection of a membrane potential in purified virions and this was enhanced by a regulator of the tricarboxylic acid cycle but abolished by the use of a depolarizing agent. Bioinformatics was employed to identify enzymes involved in virion proton gradient generation and this approach revealed that 8 putative P. massiliensis proteins exhibited low sequence identities with known cellular enzymes involved in the universal tricarboxylic acid cycle. Further, all 8 viral genes were transcribed during replication. The product of one of these genes, ORF132, was cloned and expressed in Escherichia coli, and shown to function as an isocitrate dehydrogenase, a key enzyme of the tricarboxylic acid cycle. Our findings show for the first time that a membrane potential can exist in Pandoraviruses, and this may be related to tricarboxylic acid cycle. The presence of a proton gradient in P. massiliensis makes this virus a form of life for which it is legitimate to ask the question ‘what is a virus?’.
published_date 2022-03-01T04:13:59Z
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