Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family

The evolutionary origins of arboviruses are unknown because their typical dual host tropism is paraphyletic within viral families. Here we studied one of the most diversified and medically relevant RNA virus families, the Bunyaviridae, in which four of five established genera are transmitted by arth...

Full description

Saved in:
Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 24; pp. 7536 - 7541
Main Authors: Marklewitz, Marco, Zirkel, Florian, Kurth, Andreas, Drosten, Christian, Junglen, Sandra
Format: Journal Article
Language:English
Published: United States 16.06.2015
Subjects:
Amino Acid Sequence
Animals
Arboviruses - classification
Arboviruses - genetics
Arboviruses - pathogenicity
Base Sequence
Bunyaviridae - classification
Bunyaviridae - genetics
Bunyaviridae - pathogenicity
Cell Line
Conserved Sequence
Culicidae - virology
Endonucleases - genetics
Evolution, Molecular
Genome, Viral
Host Specificity
Microscopy, Electron
Molecular Sequence Data
Phenotype
Phylogeny
RNA Replicase - genetics
RNA, Viral - genetics
Sequence Homology, Amino Acid
Species Specificity
Temperature
Viral Proteins - genetics
ancestral reconstruction
insect-specific virus
bunyavirus
virus evolution
arbovirus
ISSN:1091-6490
Online Access:Get more information
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary:The evolutionary origins of arboviruses are unknown because their typical dual host tropism is paraphyletic within viral families. Here we studied one of the most diversified and medically relevant RNA virus families, the Bunyaviridae, in which four of five established genera are transmitted by arthropods. We define two cardinally novel bunyavirus groups based on live isolation of 26 viral strains from mosquitoes (Jonchet virus [JONV], eight strains; Ferak virus [FERV], 18 strains). Both viruses were incapable of replicating at vertebrate-typical temperatures but replicated efficiently in insect cells. Replication involved formation of virion-sense RNA (vRNA) and mRNA, including cap-snatching activity. SDS/PAGE, mass spectrometry, and Edman degradation identified translation products corresponding to virion-associated RNA-dependent RNA polymerase protein (RdRp), glycoprotein precursor protein, glycoproteins Gn and Gc, as well as putative nonstructural proteins NSs and NSm. Distinct virion morphologies suggested ancient evolutionary divergence, with bunyavirus-typical morphology for FERV (spheres of 60-120 nm) as opposed to an unusual bimorphology for JONV (tubular virions of 60 × 600 nm and spheres of 80 nm). Both viruses were genetically equidistant from all other bunyaviruses, showing <15% amino acid identity in the RdRp palm domain. Both had different and unique conserved genome termini, as in separate bunyavirus genera. JONV and FERV define two novel sister taxons to the superclade of orthobunyaviruses, tospoviruses, and hantaviruses. Phylogenetic ancestral state reconstruction with probabilistic hypothesis testing suggested ancestral associations with arthropods at deep nodes throughout the bunyavirus tree. Our findings suggest an arthropod origin of bunyaviruses.
Bibliography:ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ISSN:1091-6490
DOI:10.1073/pnas.1502036112