A multicellular way of life for a multipartite virus.

Anne Sicard,Yannis Michalakis,Marie-Stéphanie Vernerey,Stéphane Blanc,Romain Gallet,Cica Urbino,Michel Peterschmitt,Serafin Gutierrez,Michel Yvon,Elodie Pirolles

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.

Highlights

Viruses introduce their genome into a susceptible cell and highjack diverse cell functions to complete their replication cycle
In our specific experimental model species, we demonstrate that the distinct segments do not need be together in individual cells for the system to be functional
We first compared the localization of distinct segments in individual cells of faba bean host plants with specific fluorescent probes and confocal microscopy

Summary

Introduction

Viruses introduce their genome into a susceptible cell and highjack diverse cell functions to complete their replication cycle. Depending on the viral species, multipartite viruses have their genome composed of two to eight segments of DNA or RNA (single or double stranded), each encapsidated individually in a separate virus particle. Microbiology and Infectious Disease eLife digest Many viruses are small particles consisting of genetic material surrounded by a coat made of proteins They are unable to multiply on their own and so they must enter a host cell and trick it into reading their genetic information to produce new virus particles. There is a low probability that a single cell could be infected with all eight different types of particle at the same time and receive the complete FBNSV genome How is this virus able to successfully multiply within a plant?. They accumulate independently in and complement across neighboring cells, defining a multicellular way of life

Results

Materials and methods

Funding Funder