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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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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
Online Access: Check full text

URI: https://cronfa.swan.ac.uk/Record/cronfa57909
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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 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?’.
Keywords: giant viruses; Pandoravirus; energy metabolism; ATP production; Lipman 25 system; tricarboxylic acid cycle
College: Swansea University Medical School
Funders: 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).
Issue: 3
Start Page: 695
End Page: 704