Multipartite viruses: Organization, emergence and evolution

Viruses are among the simplest replicative entities on Earth. They are obligate intracelllular parasites that typically form large and fast-evolving populations. Beyond their high mutation rates, viruses deploy a number of adaptive strategies unseen in cellular organisms. Inside the cell, complementation among genomes is a common strategy that often permits variants of low fitness with incomplete genomes to thrive in the population. Complementation between viral genomes seems to be taken to its ultimate consequences in the case of multipartite viruses: the genome of these viruses is fragmented and encapsidated into independent viral particles. Since all the genomic segments have to meet in the host for complementation, multipartite viruses are bound to fight the loss of genomic information.The need for coinfection or complementation demands a high viral density that is difficult to achieve in nature. While this is an obvious disadvantage of this strategy, no consensus on its actual advantages has been reached. What is more, the main open question about multipartite viruses is why they exist at all. In order to contribute to the understanding of this viral strategy, we quantify the prevalence of multipartite viruses by analysing publicly available databases. Amongst their outstanding characteristics, we found that a non-negligible amount of all annotated viral species are multipartite, and most of them infect plants. Although it is generally assumed that multipartitism is viable only when propagation occurs at high viral density, evidence indicates that severe population bottlenecks are common, especially for plant viruses. Therefore, we investigate the effect of genome segmentation as an evolutionary pressure that favours multipartite over monopartite populations through complementation. We consider a situation where incomplete genomes are generated through errors in the replication of a monopartite wild type virus and determine how their maintenance is constrained by viral density. Propagation of infection in plants is strongly conditioned by the structured nature of plant tissues, which alleviate the requirement of complementation by favouring local clustering. As a result, we observe that in spatial competition multipartite viral forms can displace monopartite counterparts under less restrictive environmental conditions. Taking an ecological viewpoint of the Virosphere, infections result from an ensemble of interacting viruses and subviral entities. Satellites are subviral entities that rely on a helper virus for replication and maintenance. In return, satellites open up a new range of infection phenotypes. Virus-satellite coinfections are ubiquitous in plant infections and less common in other hosts. The ecological outcomes of these associations may compensate for the cost of coinfection and we conjecture that they represent a plausible first step towards multipartitism. We present a dynamical system for the competition between two viruses, one of them assisted by a satellite, and find solutions where the tandem virus-satellite prevails despite the requirement of coinfection. The genomic segments composing multipartite genomes are, in principle, indistinguishable from those of other viruses; however, as a plant virus, their origin might be linked with the expansion of RNA viruses during the flourishing of eukaryotic cells. The evolution of eukaryotic viruses is highly relying on a modular constructive principle, mostly driven by extensive horizontal gene transfer. We placed the origin of multipartitism in the global phylogeny of RNA viruses and found outstanding features in their evolution. Multipartitism has repeatedly emerged along the evolution and diversification of RNA viruses, possibly driven by a constructive principle that enhances gene sharing within this group as compared to the rest of viruses. In summary, we propose plausible mechanistic and evolutionary origins of different families of multipartite viruses and hypothesize that the power of multipartitism relies on its plasticity and, at the same time, unavoidably in an ecological context. It is only by exploring the interplay between evolution and ecology that we can elucidate the possible and the actual in viral adaptive strategies.