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 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 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. It is generally thought that the process of making new virus particles happens independently in each infected cell. This idea assumes that a given particle contains the entire set of genetic material (known as the genome) of that virus, but this is not always the case. Many so-called ‘multipartite’ viruses have genomes that are split into several segments carried in separate particles: in this case, a single particle only contains a portion of the entire viral genome. Faba bean necrotic stunt virus (or FBNSV for short) is a multipartite virus that infects and causes disease in members of the pea and bean family. There are eight types of FBNSV particle that each carries a distinct genome segment, a small section of the entire viral genome. 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. So how is this virus able to successfully multiply within a plant? To address this question, Sicard et al. used microscopy to study FBNSV genome segments as they infected the cells of faba bean plants. The experiments confirmed that the eight different segments of the FBNSV genome were not necessarily found together within the same cell, but instead accumulated independently in different cells. This means that a cell infected with FBNSV may be unable to make all of the proteins needed to assemble new virus particles. However, additional experiments demonstrated that infected cells may be exchanging virus proteins, which could enable them to create complete virus particles. The findings of Sicard et al. demonstrate that FBNSV hijacks groups of host cells to manufacture new virus particles, rather than relying on individual cells as previously thought. It is possible that other multipartite and non-multipartite viruses work a similar manner. Ultimately, this knowledge may reshape what we know about how viruses infect their hosts.