Review Article | Published:

Mimivirus: leading the way in the discovery of giant viruses of amoebae

Nature Reviews Microbiology volume 15, pages 243254 (2017) | Download Citation

Abstract

The accidental discovery of the giant virus of amoeba — Acanthamoeba polyphaga mimivirus (APMV; more commonly known as mimivirus) — in 2003 changed the field of virology. Viruses were previously defined by their submicroscopic size, which probably prevented the search for giant viruses, which are visible by light microscopy. Extended studies of giant viruses of amoebae revealed that they have genetic, proteomic and structural complexities that were not thought to exist among viruses and that are comparable to those of bacteria, archaea and small eukaryotes. The giant virus particles contain mRNA and more than 100 proteins, they have gene repertoires that are broader than those of other viruses and, notably, some encode translation components. The infection cycles of giant viruses of amoebae involve virus entry by amoebal phagocytosis and replication in viral factories. In addition, mimiviruses are infected by virophages, defend against them through the mimivirus virophage resistance element (MIMIVIRE) system and have a unique mobilome. Overall, giant viruses of amoebae, including mimiviruses, marseilleviruses, pandoraviruses, pithoviruses, faustoviruses and molliviruses, challenge the definition and classification of viruses, and have increasingly been detected in humans.

Key points

  • Acanthamoeba polyphaga mimivirus (APMV) and subsequently discovered giant viruses of amoebae challenge the previous definition of viruses and their classification.

  • The replication cycle, structure, genomic make-up and plasticity of giant viruses differ from those of traditional viruses. They extend the definition of viruses into a broader range of biological entities, some of which are very simple and others of which have a complexity that is comparable to that of other microorganisms.

  • Giant viruses of amoebae have virus particles as large as some microorganisms that are visible by light microscopy and that have a stunning level of complexity. Their genomes are mosaics and contain large repertoires of genes, some of which are hallmarks of cellular organisms, although the majority of which have unknown functions.

  • Mimiviruses are associated with a specific mobilome and are parasitized by viruses that they can defend against.

  • Several hypotheses on the ancient origin and evolutionary relationship between cellular organisms and giant viruses of amoebae have been proposed, and these topics continue to be debated.

  • The detection of giant viruses of amoebae in humans and the study of their potential pathogenicity are emerging fields.

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Acknowledgements

The authors thank I. Pagnier, J. Bou Khalil and J. Andreani for providing electron microscopy images.

Author information

Affiliations

  1. Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), Aix-Marseille University, UM63, CNRS 7278, IRD 198, INSERM 1095, Institut Hospitalo-Universitaire (IHU) - Méditerranée Infection, AP-HM, 19–21 Boulevard Jean Moulin, 13385 Marseille, France.

    • Philippe Colson
    • , Bernard La Scola
    • , Anthony Levasseur
    •  & Didier Raoult
  2. Evolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois, 332 National Soybean Research Center, 1101 West Peabody Drive, Urbana, Illinois 61801, USA.

    • Gustavo Caetano-Anollés

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Didier Raoult.

Supplementary information

PDF files

  1. 1.

    Supplementary information S1 (table)

    Criteria for the definition of viruses and the applicability to Mimivirus and other giant viruses of amoebas1,2,3

  2. 2.

    Supplementary information S2 (figure)

    Schematic structure of Mimivirus

  3. 3.

    Supplementary information S3 (table)

    List of major representatives of mimiviruses and other giant viruses of amoebas and virophages

  4. 4.

    Supplementary information S4 (figure)

    Worldwide distribution of giant viruses of amoebae and virophages isolated by amoebal co-culture from environmental samples

  5. 5.

    Supplementary information S5 (table)

    Discovery and major features of giant viruses of amoebae (apart from mimiviruses)

  6. 6.

    Supplementary information S6 (figure)

    Main features of giant viruses of amoebae that are prototype members for described viral families or represent new putative viral families

  7. 7.

    Supplementary information S7 (figure)

    Comparisons of giant viruses of amoebae based on their genome size, virion size, and G+C, gene and ORFan content

Glossary

Virophages

Viruses that depend on the co-infection of their amoebal host by mimiviruses. Virophages replicate within mimivirus factories.

Transpovirons

Transposable elements that are 7 kb long and contain long terminal inverted repeats.

Mimivirus virophage resistance element

(MIMIVIRE). A viral defence system that confers a nucleic-acid-based immunity against virophage infection.

Fourth domain

A suggested additional domain to the three domains of life (Bacteria, Archaea and Eukarya) that were proposed by Woese. The term was initially coined in 2010.

TRUC

(Things resisting uncompleted classifications). A term that was coined in 2013 and proposes an alternative classification of microorganisms to the one that is based on ribosomal genes, which groups giant viruses in a fourth TRUC of microorganisms.

Double jelly-roll fold

A protein fold that is found exclusively in double-stranded DNA viruses and is comprised of two connected single jelly-roll folds, which are composed of eight β-strands arranged in two four-stranded sheets.

Orphan genes

Genes that lack a homologue in any sequence database.

Mobilome

This term represents the mobile genetic elements in the mimivirus genome and corresponds to provirophages and transpovirons, in addition to inteins and introns.

Monophyletic clade

A group of organisms, or taxon, that consists of all of the descendants of an ancestral species.

Phagocytosis

The engulfment of a solid particle by a cell, which forms an internal compartment named a phagosome.

Mosaicism

Applied to microbial genomes, this term is used to describe the coexistence in a genome of genes with different origins (viral, bacteria, archaeal or eukaryotic) as the result of lateral gene transfers.

Permafrost

Rock or soil at a temperature equal to, or below, 0 °C for two or more years. Permafrost is mainly located in and around the Arctic and Antarctic regions.

dN/dS ratio

A ratio of the number, over a given period of time, of non-synonymous substitutions per non-synonymous site (dN) to the number of synonymous substitutions per synonymous site (dS), which quantifies selection pressures.

Viral factories

Structural and functional elements that are associated with the replication of viral nucleic acids and the substantial production of virus particles.

Exocytosis

Active transport of molecules, such as proteins, out of a cell through a process that uses energy.

Sympatric

Inhabiting the same ecological niche.

Seroconversion

The development of antibodies in the blood that are specifically directed against an infectious agent and become detectable by serological tests.

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DOI

https://doi.org/10.1038/nrmicro.2016.197

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