The Complex Nature of Tupanviruses

Rodrigues, Rodrigo Araújo Lima; Arantes, Thalita Souza; Oliveira, Graziele Pereira; Silva, Ludmila Karen dos Santos; Abrahão, Jônatas Santos

doi:10.1016/bs.aivir.2018.09.001

Cited by 20 publications

(18 citation statements)

References 110 publications

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“…Moreover, tupanviruses also harbor a gene coding for citrate synthase (13). Recent data indicate that some giant viruses could have genes that are involved in metabolic pathways such as fermentation, sphingolipid biosynthesis and nitrogen metabolism (14).…”

Section: Introductionmentioning

confidence: 99%

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

Aherfi

Belhaouari

Pinault

et al. 2020

Preprint

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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?’.

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Section: Introductionmentioning

confidence: 99%

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

Aherfi

Belhaouari

Pinault

et al. 2020

Preprint

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“…Tupanvirus Deep Ocean and Tupanvirus Soda Lake were found in ocean sediments and soda lake samples collected in Brazil, respectively. According to their distinct structural, genetic, and biologic features, these two giant viruses were classified as distant mimivirus relatives and have been proposed to be part of a new genus Tupanvirus 17,18 . Here, we report, for the first time to our knowledge, a preliminary identification of a mechanism of cross-species transmission of virophages to infect these giant viruses.…”

mentioning

confidence: 99%

A virophage cross-species infection through mutant selection represses giant virus propagation, promoting host cell survival

et al. 2020

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Virus adaptation to new hosts is a major cause of infectious disease emergence. This mechanism has been intensively studied in the context of zoonotic virus spillover, due to its impact on global health. However, it remains unclear for virophages, parasites of giant viruses and potential regulators of microbial communities. Here, we present, for the first time to our knowledge, evidence of cross-species infection of a virophage. We demonstrated that challenging the native population of Guarani virophage with two previously unidentified giant viruses, previously nonpermissive to this virophage, allows the selection of a mutant genotype able to infect these giant viruses. We were able to characterize the potential genetic determinant (deletion) carried by the virophage with the expanded-host range. Our study also highlights the relevant biological impact of this host adaptation by demonstrating that coinfection with the mixture containing the mutant virophage abolishes giant virus production and rescues the host cell population from lysis.

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“…Tupanvirus is one of the most complex viruses isolated to date 22 . In addition to the distinct genetic and structural characteristics of this virus, it exhibits a remarkable biological feature never previously observed in other giant viruses.…”

Section: Tupanvirus-induced Host-ribosomal Shutdown Prevents Virophagmentioning

confidence: 99%

“…In this study, two recently isolated distant mimiviruses, known as Tupanvirus Deep Ocean and Tupanvirus Soda Lake, were challenged with virophages [20][21][22] . We report a preliminary identification of the first mechanism of host range expansion in virophages.…”

Section: Introductionmentioning

confidence: 99%

First evidence of host range expansion in virophages and its potential impact on giant viruses and host cells

Mougari

Chelkha

Sahmi-Bounsiar

et al. 2019

Preprint

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Virophages are satellite-like double stranded DNA viruses whose replication requires the presence of two biological entities, a giant virus and a protist. In this report, we present the first evidence of host range expansion in a virophage. We demonstrated that the Guarani virophage was able to spontaneously expand its viral host range to replicate with two novel giant viruses that were previously nonpermissive to this virophage. We were able to characterize a potential genetic determinant of this cross-species infection. We then highlighted the relevant impact of this host adaptation on giant viruses and protists by demonstrating that coinfection with the mutant virophage abolishes giant virus production and rescues the host cell population from lysis. The results of our study help to elucidate the parasitic lifestyle of virophages and their interactions with giant viruses and protists. author/funder. All rights reserved. No reuse allowed without permission.

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The Complex Nature of Tupanviruses

Cited by 20 publications

References 110 publications

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

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

A virophage cross-species infection through mutant selection represses giant virus propagation, promoting host cell survival

First evidence of host range expansion in virophages and its potential impact on giant viruses and host cells

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