Novel tri-segmented rhabdoviruses: A data mining expedition unveils the cryptic diversity of cytorhabdoviruses

Abstract

Cytorhabdoviruses (genusCytorhabdovirus, familyRhabdoviridae) are plant-infecting viruses with enveloped, bacilliform virions. Established members of the genusCytorhabdovirushave unsegmented single-stranded negative-sense RNA genomes (ca. 10-16 kb) which encode four to ten proteins. Here, by exploring large publicly available metatranscriptomics datasets, we report the identification and genomic characterization of 93 novel viruses with genetic and evolutionary cues of cytorhabdoviruses. Strikingly, five unprecedented cytorhabdoviruses with tri-segmented genomes were also identified. This finding represents the first tri-segmented viruses in the familyRhabdoviridae. Interestingly, the nucleocapsid and polymerase were the only typical rhabdoviral proteins encoded by those tri-segmented viruses, whereas in three of them, a protein similar to the emaravirus (familyFimoviridae) silencing suppressor was found, while the other predicted proteins had no matches in any sequence databases. Genetic distance and evolutionary insights suggest that all these novel viruses may represent members of novel species. Phylogenetic analyses, of both novel and previously classified plant rhabdoviruses, provide compelling support for the division of the genusCytorhabdovirusinto three distinct genera. This proposed reclassification not only enhances our understanding of the evolutionary dynamics within this group of plant rhabdoviruses but also illuminates the remarkable genomic diversity they encompass. This study not only represents a significant expansion of genomics of cytorhabdoviruses that will enable future research on the evolutionary peculiarity of this genus, but also shows the plasticity in the rhabdovirus genome organization with the discovery of tri-segmented members with a unique evolutionary trajectory.

Insights into the RNA virome of the corn leafhopperDalbulus maidis, a major emergent threat of Maize in Latin America

“…Tentative virus-like contigs were curated (extended and/or confirmed) by iterative mapping of each SRA library's filtered reads. This strategy was used to extract a subset of reads related to the query contig, used the retrieved reads from each mapping to extend the contig and then repeat the process iteratively using as query the extended sequence [27]. The extended and polished transcripts were reassembled using Geneious v8.1.9 (Biomatters Ltd.) alignment tool with high sensitivity parameters.…”

“…Rhabdoviridae is a family of negative-sense single-stranded RNA (-ssRNA) viruses with a monopartite genome as a hallmark of almost all rhabdoviruses. However, plant-associated rhabdoviruses with bi-segmented and tri-segmented genomes have been described [27,57] . Members belonging to the Rhabdoviridae family are highly diverse and have a wide host range and a great genome complexity and many members of this family have been discovered in many insect species, some of which may serve as unique hosts or may act as biological vectors for transmission to other animals or plants [12,57,58].…”