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Cited by 15Bacteriophages and microbial interactionsPlant and Fungal Interactions ResearchViral Infectious Diseases and Gene Expression in Insects

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Functional redundancy revealed by the deletion of the mimivirus GMC-oxidoreductase genes

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Alempic, Jean-Marie, Bisio, Hugo, Villalta, Alejandro, Santini, Sébastien, Lartigue, Audrey, Schmitt, Alain, Bugnot, Claire, Notaro, Anna, Belmudes, Lucid, Adrait, Annie, Poirot, Olivier, Ptchelkine, Denis, De Castro, Cristina, Couté, Yohann, Abergel, Chantal·2024·microLife
DOI 10.1093/femsml/uqae006PMC PMC11042495

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Abstract

The mimivirus 1.2 Mb genome was shown to be organized into a nucleocapsid-like genomic fiber encased in the nucleoid compartment inside the icosahedral capsid. The genomic fiber protein shell is composed of a mixture of two GMC-oxidoreductase paralogs, one of them being the main component of the glycosylated layer of fibrils at the surface of the virion. In this study, we determined the effect of the deletion of each of the corresponding genes on the genomic fiber and the layer of surface fibrils. First, we deleted the GMC-oxidoreductase, the most abundant in the genomic fiber, and determined its structure and composition in the mutant. As expected, it was composed of the second GMC-oxidoreductase and contained 5- and 6-start helices similar to the wild-type fiber. This result led us to propose a model explaining their coexistence. Then we deleted the GMC-oxidoreductase, the most abundant in the layer of fibrils, to analyze its protein composition in the mutant. Second, we showed that the fitness of single mutants and the double mutant were not decreased compared with the wild-type viruses under laboratory conditions. Third, we determined that deleting the GMC-oxidoreductase genes did not impact the glycosylation or the glycan composition of the layer of surface fibrils, despite modifying their protein composition. Because the glycosylation machinery and glycan composition of members of different clades are different, we expanded the analysis of the protein composition of the layer of fibrils to members of the B and C clades and showed that it was different among the three clades and even among isolates within the same clade. Taken together, the results obtained on two distinct central processes (genome packaging and virion coating) illustrate an unexpected functional redundancy in members of the family Mimiviridae, suggesting this may be the major evolutionary force behind their giant genomes.

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Metadata

Authors
Alempic, J.-M., Bisio, H., Villalta, A., Santini, S., Lartigue, A., Schmitt, A., Bugnot, C., Notaro, A., Belmudes, L., Adrait, A., Poirot, O., Ptchelkine, D., De Castro, C., Couté, Y., & Abergel, C.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • University of Naples Federico II (IT)
  • Department of Agricultural Sciences, University of Naples Federico II , Via Università 100, 80055 Portici ,
Corresponding author
Abergel, Chantal
ORCID
Venue
microLife
Publisher
Oxford University Press (OUP)
Published
2024
Volume
5
Pages
uqae006-uqae006
ISSN
2633-6693 (ISSN-L)
DOI
10.1093/femsml/uqae006
PMC
PMC11042495
OpenAlex
W4393977842
Cited by
15
References
2
Citations by year
2026: 3 · 2025: 9 · 2024: 3
FWCI
4.10
Type
journal article
Language
en
Open access
Licence
Locations
  • microLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
Funders
European Research Council (832 601)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Immunology and Microbiology › Virology › Plant and Fungal Interactions Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Viral Infectious Diseases and Gene Expression in Insects
Keywords
Mimivirus, functional redundancy, deletion mutants, genome packaging, viral assembly, Mimiviridae, giant viruses, protein paralogs, helical conformation, glycan composition, viral clades

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