Multipartite viruses have a strange lifestyle. Their genome is split up into different viral particles that, in principle, propagate independently. Completing the replication cycle, however, requires the full genome such that persistent infection of a host requires the concurrent presence of all types of particles. The origin of multipartite viruses is an evolutionary puzzle. Apart from why they can have such a costly lifestyle, the most peculiar thing about them is that almost all known multipartite viruses infect either plants or fungi — very few viral species infect animals.
So far, most theoretical research has been trying to focus on explaining how it is viable to have the genome split into different particles. This paper provides a theoretical explanation of why multipartite viruses primarily infect plants.
There have been great efforts to understand the mechanisms that give multipartite viruses an advantage that can compensate for their peculiar and costly lifestyle, and this is not yet a solved problem. In addition, our understanding of why most multipartite viruses infect only plants is limited. In a recent work, published in Physical Review Letters, Petter Holme of the World Research Hub Initiative, Tokyo Tech, and colleagues from China and the USA, have explained why multipartite viruses primarily infect plants. In their work, the authors formulated a minimal network-epidemiological model.
They used mathematical models and computer simulations to show that multipartite viruses colonize a structured population (representing the interaction patterns among plants) with less resistance, compared to a well-mixed population (representing the interaction patterns among animals). This is thus an explanation of why multipartite viruses infect plants rather than animals.
The researchers from Tokyo Tech continue to investigate the epidemiology of different types of infectious diseases by theoretical methods. At the moment, they are interested in the more common disease spreading scenarios such as how influenza spreads in cities and how that could be mitigated.
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 nano-virus 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 nano viruses) where the infection can operate at a level above the individual cell level, defining a viral multicellular way of life.
Distinct segments accumulate independently in distinct individual host cells
One may argue, sticking to the paradigm that the viral genetic information is replicated as an integral genome within individual cells, that all FBNSV segments are present in infected cells but that the apparent absence of some in Figure 1 is due to the detection limit of our technique. Because every technique has its limit, whatever the technology implemented, it would not be reasonable to certify that the absence of detection is proof of the absence of the corresponding segment. We thus imagined an approach where the detection limit becomes irrelevant. For a given pair of segments, we quantified and compared both green and red fluorescence in all individual cells where at least one of the two was observed above background (for detailed quantification procedure see the Materials and methods section). By doing so, we alleviate the problem of the limit of detection and rather question whether the accumulation of one segment of the pair is dependent on that of the other. As a positive control of this approach, we first produced two fluorescent probes, each specifically labeling a different region of the same segment R (probes R1 and R2). Figure 2 illustrates that all cells labeled by R1 are also labeled by R2 (Figure 2A). Moreover, plotting the average intensity of green over red fluorescence for each of these cells resulted in a highly significant linear relationship (correlation coefficient r = 0.90, p=1.98 10−23 in the example of petiole N° 42 in Figure 2B). Four independent repeats of this control similarly showed strong correlations (Table 1). This result validates our approach by demonstrating that when we monitor two viral DNA sequences whose accumulation should be highly correlated, such as two regions of the same segment, we indeed find that they co-localize and accumulate at highly correlated levels.