Date Published: November 3, 2016
Publisher: Public Library of Science
Author(s): Anne Sicard, Yannis Michalakis, Serafín Gutiérrez, Stéphane Blanc, Tom C. Hobman.
Multipartite viruses have one of the most puzzling genetic organizations found in living organisms. These viruses have several genome segments, each containing only a part of the genetic information, and each individually encapsidated into a separate virus particle. While countless studies on molecular and cellular mechanisms of the infection cycle of multipartite viruses are available, just as for other virus types, very seldom is their lifestyle questioned at the viral system level. Moreover, the rare available “system” studies are purely theoretical, and their predictions on the putative benefit/cost balance of this peculiar genetic organization have not received experimental support. In light of ongoing progresses in general virology, we here challenge the current hypotheses explaining the evolutionary success of multipartite viruses and emphasize their shortcomings. We also discuss alternative ideas and research avenues to be explored in the future in order to solve the long-standing mystery of how viral systems composed of interdependent but physically separated information units can actually be functional.
The architecture, organization, and packaging of viral genetic information can be divided into three categories: monopartite, segmented, and multipartite viruses. Monopartite viruses have a single nucleic acid molecule protected in a shell made of proteins (and sometimes also lipids) forming the virus particle. The genome of segmented viruses is divided into two or more nucleic acid segments that are all encapsidated together in a single virus particle. Multipartite viruses (the terms multicomponent viruses and coviruses are also used in the literature) have their genome divided into two or more nucleic acid segments, just as the segmented type, but these segments are each packaged into separate virus particles. This latter peculiar organization is the only one resulting in viral transmissible entities that do not contain the entire genetic information, and in which the co-transmission of several virus particles to a new cell or host appears mandatory to maintain the integrity of the viral genome. The biology of multipartite viruses challenges some basic concepts of virology and evolution, and, at this point, it remains hard (if possible at all) to conceive how they have evolved and how they can actually be functional.