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Tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: Is it still a virus?

Sarah Aherfi, Djamal Brahim Belhaouari, Lucile Pinault, Jean-Pierre Baudoin, Philippe Decloquement, Jonatas Abrahao, Philippe Colson, Anthony Levasseur, David C. Lamb, Eric Chabriere, Didier Raoult, Bernard La Scola
doi: https://doi.org/10.1101/2020.09.21.306415
Sarah Aherfi
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Djamal Brahim Belhaouari
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Lucile Pinault
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Jean-Pierre Baudoin
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Philippe Decloquement
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Jonatas Abrahao
2Laboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
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Philippe Colson
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Anthony Levasseur
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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David C. Lamb
3Institute of Life Science and School of Medicine, Swansea University, Swansea SA2 8PP, United Kingdom
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Eric Chabriere
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Didier Raoult
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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Bernard La Scola
1Aix-Marseille Université, Institut de Recherche pour le Développement (IRD), Assistance Publique - Hôpitaux de Marseille (AP-HM); Microbes, Evolution, Phylogeny and Infection (MEΦI); Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, 19-21 boulevard Jean Moulin, 13005 Marseille, France
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  • For correspondence: bernard.la-scola@univ-amu.fr
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ABSTRACT

Since the discovery of Acanthamoeba polyphaga Mimivirus, the first giant virus of amoeba, the historical hallmarks defining a virus have been challenged. Giant virion sizes can reach up to 2.3 µm, making them visible by optical microscopy. They have large genomes of up to 2.5 Mb that encode proteins involved in the translation apparatus. Herein, we investigated possible energy production in Pandoravirus massiliensis, the largest of our giant virus collection. MitoTracker and TMRM mitochondrial membrane markers allowed for the detection of a membrane potential in virions that could be abolished by the use of the depolarizing agent CCCP. An attempt to identify enzymes involved in energy metabolism revealed that 8 predicted proteins of P. massiliensis exhibited low sequence identities with defined proteins involved in the universal tricarboxylic acid cycle (acetyl Co-A synthase; citrate synthase; aconitase; isocitrate dehydrogenase; α-ketoglutarate decarboxylase; succinate dehydrogenase; fumarase). All 8 viral predicted ORFs were transcribed together during viral replication, mainly at the end of the replication cycle. Two of these proteins were detected in mature viral particles by proteomics. The product of the ORF132, a predicted protein of P. massiliensis, cloned and expressed in Escherichia coli, provided a functional isocitrate dehydrogenase, a key enzyme of the tricarboxylic acid cycle, which converts isocitrate to α-ketoglutarate. We observed that membrane potential was enhanced by low concentrations of Acetyl-CoA, a regulator of the tricarboxylic acid cycle. Our findings show for the first time that energy production can occur in viruses, namely, pandoraviruses, and the involved enzymes are related to tricarboxylic acid cycle enzymes. The presence of a proton gradient in P. massiliensis coupled with the observation of genes of the tricarboxylic acid cycle make this virus a form a life for which it is legitimate to question ‘what is a virus?’.

Competing Interest Statement

This work was supported by the French Government under the "Investments for the Future" program managed by the National Agency for Research (ANR) Mediterranee-Infection 10-IAHU-03. It was also supported by Region PACA and European funding FEDER PRIMMI.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted September 21, 2020.
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Tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: Is it still a virus?
Sarah Aherfi, Djamal Brahim Belhaouari, Lucile Pinault, Jean-Pierre Baudoin, Philippe Decloquement, Jonatas Abrahao, Philippe Colson, Anthony Levasseur, David C. Lamb, Eric Chabriere, Didier Raoult, Bernard La Scola
bioRxiv 2020.09.21.306415; doi: https://doi.org/10.1101/2020.09.21.306415
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Tricarboxylic acid cycle and proton gradient in Pandoravirus massiliensis: Is it still a virus?
Sarah Aherfi, Djamal Brahim Belhaouari, Lucile Pinault, Jean-Pierre Baudoin, Philippe Decloquement, Jonatas Abrahao, Philippe Colson, Anthony Levasseur, David C. Lamb, Eric Chabriere, Didier Raoult, Bernard La Scola
bioRxiv 2020.09.21.306415; doi: https://doi.org/10.1101/2020.09.21.306415

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