1. Microbiology and Infectious Disease
Download icon

A multicellular way of life for a multipartite virus

  1. Anne Sicard
  2. Elodie Pirolles
  3. Romain Gallet
  4. Marie-Stéphanie Vernerey
  5. Michel Yvon
  6. Cica Urbino
  7. Michel Peterschmitt
  8. Serafin Gutierrez
  9. Yannis Michalakis
  10. Stéphane Blanc  Is a corresponding author
  1. INRA, Centre Occitanie Montpellier, France
  2. Centre National de la Recherche Scientifique, France
Short Report
  • Cited 16
  • Views 16,726
  • Annotations
Cite this article as: eLife 2019;8:e43599 doi: 10.7554/eLife.43599

Abstract

A founding paradigm in virology is that the spatial unit of the viral replication cycle is an individual cell. Multipartite viruses have a segmented genome where each segment is encapsidated separately. In this situation the viral genome is not recapitulated in a single virus particle but in the viral population. How multipartite viruses manage to efficiently infect individual cells with all segments, thus with the whole genome information, is a long-standing but perhaps deceptive mystery. By localizing and quantifying the genome segments of a nanovirus in host plant tissues we show that they rarely co-occur within individual cells. We further demonstrate that distinct segments accumulate independently in different cells and that the viral system is functional through complementation across cells. Our observation deviates from the classical conceptual framework in virology and opens an alternative possibility (at least for nanoviruses) where the infection can operate at a level above the individual cell level, defining a viral multicellular way of life.

Article and author information

Author details

  1. Anne Sicard

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Elodie Pirolles

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Romain Gallet

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Marie-Stéphanie Vernerey

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Michel Yvon

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Cica Urbino

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Michel Peterschmitt

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Serafin Gutierrez

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Yannis Michalakis

    MIVEGEC (CNRS/IRD/UM), Centre National de la Recherche Scientifique, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1929-0848
  10. Stéphane Blanc

    UMR BGPI, INRA, Centre Occitanie Montpellier, Montpellier, France
    For correspondence
    stephane.blanc@inra.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3412-0989

Funding

Institut National de la Recherche Agronomique

  • Anne Sicard
  • Elodie Pirolles
  • Romain Gallet
  • Marie-Stéphanie Vernerey
  • Michel Yvon
  • Serafin Gutierrez
  • Stéphane Blanc

Centre National de la Recherche Scientifique

  • Elodie Pirolles
  • Yannis Michalakis

Institut de Recherche pour le developpement

  • Yannis Michalakis

Agence Nationale de la Recherche (ANR-14-CE02-0014)

  • Anne Sicard
  • Elodie Pirolles
  • Romain Gallet
  • Marie-Stéphanie Vernerey
  • Michel Yvon
  • Yannis Michalakis
  • Stéphane Blanc

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Fernando García-Arenal, Technical University of Madrid, Spain

Publication history

  1. Received: November 13, 2018
  2. Accepted: February 26, 2019
  3. Accepted Manuscript published: March 12, 2019 (version 1)
  4. Version of Record published: March 12, 2019 (version 2)

Copyright

© 2019, Sicard et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 16,726
    Page views
  • 1,309
    Downloads
  • 16
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Biochemistry and Chemical Biology
    2. Microbiology and Infectious Disease
    Masihuz Zaman, Maria Andreasen
    Research Article

    The infective ability of the opportunistic pathogen Staphylococcus aureus, recognized as the most frequent cause of biofilm-associated infections, is associated with biofilm mediated resistance to host immune response. Phenol-soluble modulins (PSM) comprise the structural scaffold of S. aureus biofilms through self-assembly into functional amyloids, but the role of individual PSMs during biofilm formation remains poorly understood and the molecular pathways of PSM self-assembly have yet to be identified. Here, we demonstrate high degree of cooperation between individual PSMs during functional amyloid formation. PSMα3 initiates the aggregation, forming unstable aggregates capable of seeding other PSMs resulting in stable amyloid structures. Using chemical kinetics we dissect the molecular mechanism of aggregation of individual PSMs showing that PSMα1, PSMα3 and PSMβ1 display secondary nucleation whereas PSMβ2 aggregates through primary nucleation and elongation. Our findings suggest that the various PSMs have solved to ensure fast and efficient biofilm formation through cooperation between individual peptides.

    1. Microbiology and Infectious Disease
    Peter C Dumoulin et al.
    Research Article

    The mechanisms underlying resistance of the Chagas disease parasite, Trypanosoma cruzi, to current therapies are not well understood, including the role of metabolic heterogeneity. We found that limiting exogenous glutamine protects actively dividing amastigotes from ergosterol biosynthesis inhibitors (azoles), independent of parasite growth rate. The antiparasitic properties of azoles are derived from inhibition of lanosterol 14α-demethylase (CYP51) in the endogenous sterol synthesis pathway. We find that carbons from 13C-glutamine feed into amastigote sterols and into metabolic intermediates that accumulate upon CYP51 inhibition. Incorporation of 13C-glutamine into endogenously synthesized sterols is increased with BPTES treatment, an inhibitor of host glutamine metabolism that sensitizes amastigotes to azoles. Similarly, amastigotes are re-sensitized to azoles following addition of metabolites upstream of CYP51, raising the possibility that flux through the sterol synthesis pathway is a determinant of sensitivity to azoles and highlighting the potential role for metabolic heterogeneity in recalcitrant T. cruzi infection.