Cargando…

A multicellular way of life for a multipartite virus

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 vir...

Descripción completa

Detalles Bibliográficos
Autores principales: Sicard, Anne, Pirolles, Elodie, Gallet, Romain, Vernerey, Marie-Stéphanie, Yvon, Michel, Urbino, Cica, Peterschmitt, Michel, Gutierrez, Serafin, Michalakis, Yannis, Blanc, Stéphane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414197/
https://www.ncbi.nlm.nih.gov/pubmed/30857590
http://dx.doi.org/10.7554/eLife.43599
_version_ 1783402947479076864
author Sicard, Anne
Pirolles, Elodie
Gallet, Romain
Vernerey, Marie-Stéphanie
Yvon, Michel
Urbino, Cica
Peterschmitt, Michel
Gutierrez, Serafin
Michalakis, Yannis
Blanc, Stéphane
author_facet Sicard, Anne
Pirolles, Elodie
Gallet, Romain
Vernerey, Marie-Stéphanie
Yvon, Michel
Urbino, Cica
Peterschmitt, Michel
Gutierrez, Serafin
Michalakis, Yannis
Blanc, Stéphane
author_sort Sicard, Anne
collection PubMed
description 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.
format Online
Article
Text
id pubmed-6414197
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-64141972019-03-14 A multicellular way of life for a multipartite virus Sicard, Anne Pirolles, Elodie Gallet, Romain Vernerey, Marie-Stéphanie Yvon, Michel Urbino, Cica Peterschmitt, Michel Gutierrez, Serafin Michalakis, Yannis Blanc, Stéphane eLife Microbiology and Infectious Disease 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. eLife Sciences Publications, Ltd 2019-03-12 /pmc/articles/PMC6414197/ /pubmed/30857590 http://dx.doi.org/10.7554/eLife.43599 Text en © 2019, Sicard et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Microbiology and Infectious Disease
Sicard, Anne
Pirolles, Elodie
Gallet, Romain
Vernerey, Marie-Stéphanie
Yvon, Michel
Urbino, Cica
Peterschmitt, Michel
Gutierrez, Serafin
Michalakis, Yannis
Blanc, Stéphane
A multicellular way of life for a multipartite virus
title A multicellular way of life for a multipartite virus
title_full A multicellular way of life for a multipartite virus
title_fullStr A multicellular way of life for a multipartite virus
title_full_unstemmed A multicellular way of life for a multipartite virus
title_short A multicellular way of life for a multipartite virus
title_sort multicellular way of life for a multipartite virus
topic Microbiology and Infectious Disease
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6414197/
https://www.ncbi.nlm.nih.gov/pubmed/30857590
http://dx.doi.org/10.7554/eLife.43599
work_keys_str_mv AT sicardanne amulticellularwayoflifeforamultipartitevirus
AT pirolleselodie amulticellularwayoflifeforamultipartitevirus
AT galletromain amulticellularwayoflifeforamultipartitevirus
AT vernereymariestephanie amulticellularwayoflifeforamultipartitevirus
AT yvonmichel amulticellularwayoflifeforamultipartitevirus
AT urbinocica amulticellularwayoflifeforamultipartitevirus
AT peterschmittmichel amulticellularwayoflifeforamultipartitevirus
AT gutierrezserafin amulticellularwayoflifeforamultipartitevirus
AT michalakisyannis amulticellularwayoflifeforamultipartitevirus
AT blancstephane amulticellularwayoflifeforamultipartitevirus
AT sicardanne multicellularwayoflifeforamultipartitevirus
AT pirolleselodie multicellularwayoflifeforamultipartitevirus
AT galletromain multicellularwayoflifeforamultipartitevirus
AT vernereymariestephanie multicellularwayoflifeforamultipartitevirus
AT yvonmichel multicellularwayoflifeforamultipartitevirus
AT urbinocica multicellularwayoflifeforamultipartitevirus
AT peterschmittmichel multicellularwayoflifeforamultipartitevirus
AT gutierrezserafin multicellularwayoflifeforamultipartitevirus
AT michalakisyannis multicellularwayoflifeforamultipartitevirus
AT blancstephane multicellularwayoflifeforamultipartitevirus