Promotion of order Bunyavirales to class Bunyaviricetes to accommodate a rapidly increasing number of related polyploviricotine viruses

Abstract

Prior to 2017, the family Bunyaviridae included five genera of arthropod and rodent viruses with tri-segmented negative-sense RNA genomes related to the Bunyamwera virus. In 2017, the International Committee on Taxonomy of Viruses (ICTV) promoted the family to order Bunyavirales and subsequently greatly expanded its composition by adding multiple families for non-segmented to polysegmented viruses of animals, fungi, plants, and protists. The continued and accelerated discovery of bunyavirals highlighted that an order would not suffice to depict the evolutionary relationships of these viruses. Thus, in April 2024, the order was promoted to class Bunyaviricetes. This class currently includes two major orders, Elliovirales (Cruliviridae, Fimoviridae, Hantaviridae, Peribunyaviridae, Phasmaviridae, Tospoviridae, and Tulasviridae) and Hareavirales (Arenaviridae, Discoviridae, Konkoviridae, Leishbuviridae, Mypoviridae, Nairoviridae, Phenuiviridae, and Wupedeviridae), for hundreds of viruses, many of which are pathogenic for humans and other animals, plants, and fungi.

Keywords: Arenaviridae; Bunyavirales; Bunyaviricetes; Cruliviridae; Discoviridae; Elliovirales; Ellioviricetes; Fimoviridae; Hantaviridae; Hareavirales; ICTV; International Committee on Taxonomy of Viruses; Konkoviridae; Leishbuviridae; Mypoviridae; Nairoviridae; Negarnaviricota; Orthornavirae; Peribunyaviridae; Phasmaviridae; Phenuiviridae; Polyploviricotina; RNA-dependent RNA polymerase; RNA-directed RNA polymerase; RdRp; Riboviria; Tospoviridae; Tulasviridae; Wupedeviridae; arenavirid; arenavirus; bunyaviral; bunyaviricete; bunyavirus; crulivirid; discovirid; ellioviral; fimovirid; fimovirus; hantavirid; hantavirus; hareaviral; konkovirid; leishbuvirid; megaclassification; megataxonomy; mypovirid; nairovirid; nairovirus; negarnaviricot; peribunyavirid; peribunyavirus; phasmavirid; phenuivirid; phenuivirus; polyploviricotine; ribovirian; tospovirid; tospovirus; tulasvirid; virus classification; virus nomenclature; virus taxonomy; wupedevirid.

Fig 1

Megataxonomic position of class Bunyaviricetes. Schematic of the megataxonomic organization of realm Riboviria down to the class rank, indicating the relative position of class Bunyaviricetes (bold, arrow). Adapted from Fig. 11A in reference (23) and Fig. 1A in reference (41).

Fig 2

Class Bunyaviricetes as of 2024. Phylogenetic tree using FastTree after MUSCLE alignment (with maxiters 100) of full-length GenBank large (L) protein (containing RNA-directed RNA polymerase domain) sequences. Highlighted are the now-established orders Elliovirales (blue) and Hareavirales (orange) and their families. Asterisks indicate unclassified viruses. Adapted from Fig. 1 in TaxoProp 2023.024M.Bunyaviricetes (40).

Fig 3

Negarnaviricot RdRp diversity. Unrooted maximum-likelihood tree (inferred with IQ-tree and the rtREV+F+R9 model) constructed with negarnaviricot RdRps available in 2021. The scale bar indicates average amino acid substitutions per site. Adapted from Fig. 10 in reference (54).