The Curious Strategy of Multipartite Viruses

Abstract

Multipartite virus genomes are composed of several segments, each packaged in a distinct viral particle. Although this puzzling genome architecture is found in ∼17% of known viral species, its distribution among hosts or among distinct types of genome-composing nucleic acid remains poorly understood. No convincing advantage of multipartitism has been identified, yet the maintenance of genomic integrity appears problematic. Here we review recent studies shedding light on these issues. Multipartite viruses rapidly modify the copy number of each segment/gene from one host species to another, a putative benefit if host switches are common. One multipartite virus functions in a multicellular way: The segments do not all need to be present in the same cell and can functionally complement across cells, maintaining genome integrity within hosts. The genomic integrity maintenance during host-to-host transmission needs further elucidation. These features challenge several virology foundations and could apply to other multicomponent viral systems.

Nine viruses from eight lineages exhibiting new evolutionary modes that co-infect a hypovirulent phytopathogenic fungus

“…The discovery of SsDFV3 demonstrates a new example for insights into the evolution of viral genome segmentation. The genomes of RNA viruses are divided into segmented or unsegmented genomes [44]. The genome segmentation from ancestral unsegmented RNA genomes probably occurred independently during viral evolution.…”

“…The actual evolutionary benefits of genome segmentation are still poorly understood; however, these events might play an important role in the evolutionary history of these viruses. Segmented viruses are generally considered to be evolved from unsegmented viruses, since segmented viruses have several survival advantages in evolution [6,[44][45][46][47]. Researchers have been trying to uncover evidence to support this conclusion.…”

Conserved Untranslated Regions of Multipartite Viruses: Natural Markers of Novel Viral Genomic Components and Tags of Viral Evolution

“…Moreover, segmented/multipartite are not rare among families or genera across virus kingdoms [1, 4]. Whether segmented/multipartite viruses are the next evolutionary steps of the monopartite viruses is still indeterminate [5]. Further, their superiorities, either confirmed, i.e., better virion stability [6] or theoretical [4, 5, 7], cannot be neglected.…”

“…Whether segmented/multipartite viruses are the next evolutionary steps of the monopartite viruses is still indeterminate [5]. Further, their superiorities, either confirmed, i.e., better virion stability [6] or theoretical [4, 5, 7], cannot be neglected. However, genomic segmentation also incurs within- and between-host costs, especially for multipartite viruses [5], despite a multicellular viral lifestyle that permits spatial segregation and possible infection delay of some components in hosts may in part counteract some of the costs [8].…”

Unresolved advantages of multipartitism in spatially structured environments

“…2013 ; Sicard et al. 2019 ; Michalakis and Blanc 2020 ). This last hypothesis links molecular advantages to ecological ones, since it involves fast adaptation to different hosts—which implicitly assumes that multipartite viral forms would be more generalist, and therefore have a larger diversity of hosts under reach due to their architecture, than monopartite or segmented species.…”