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.

COMMENTARY

In 1973, a viral family, Bunyaviridae, including one genus, Bunyavirus, was proposed to be established for numerous insect viruses based on serological cross-reactivities and similarities and differences in physical properties and virion morphologies (1). The names of these taxa were derived from the “type” virus used for all analyses, Bunyamwera virus, which was first isolated in 1946 from Aedes mosquitoes in Semliki Forest of Uganda Protectorate (2). In 1975, both family and genus were accepted by the International Committee on Taxonomy of Viruses (ICTV) (3). At the time of the family/genus proposal (1), it was already obvious that there were numerous ‘bunyavirus-like viruses’, many of them pathogenic for humans and other animals, that should be family members but should not be assigned to genus Bunyavirus. In subsequent years, additional genera were established for these ‘bunyavirus-like viruses’ and newly discovered viruses. By 1981, Bunyavirus (by then all taxon names were italicized) was joined by genera Nairovirus, Phlebovirus, and Uukuvirus to accommodate insect and tick viruses serologically related to Nairobi sheep disease virus/Crimean-Congo hemorrhagic fever virus, sandfly fever Sicilian virus, and Uukuniemi virus, respectively (4, 5). The family experienced its next major expansion when the genus Hantavirus was included for a variety of human-pathogenic rodent-borne viruses (Hantaan virus and relatives) (6). Then, in 1990, the genus Tospovirus was added for pathogenic plant viruses transmitted by thrips (tomato spotted wilt virus and relatives) (7), and the genus Uukuvirus was absorbed in the genus Phlebovirus (8).

Promotion of family Bunyaviridae to order Bunyavirales

Since 1990, improved genome sequencing methodologies, followed by increasingly efficient metagenomic sequencing and improved tools to depict phylogenies, revealed a plethora of viruses closely related to the viruses classified in the family Bunyaviridae (9–14). Yet, many of these viruses, which were found in animals, fungi, plants, and protists, could not be assigned to the established genera and those that could represent divergent clades; i.e., the three-taxon (family, genus, and species) hierarchy did not suffice to represent the diversity of the family. Consequently, in 2017, the ICTV promoted the family to order Bunyavirales and the five genera to families (Bunyavirus→Peribunyaviridae; Hantavirus→Hantaviridae; Nairovirus→Nairoviridae; Phlebovirus→Phenuiviridae; and Tospovirus→Tospoviridae) (15). In subsequent years, the order underwent repeated and substantial revisions (through the addition of numerous novel families, genera, and species) (16–22), was included in a megataxonomic framework (realm Riboviria, kingdom Orthornavirae, phylum Negarnaviricota, subphylum Polyploviricotina, class Ellioviricetes) (23–25), and was updated via the consistent application of a Latinized binomial species nomenclature (21, 22).

Establishment of class Bunyaviricetes

The continued and accelerated discovery of bunyavirals (26–36) and their RNA-directed RNA polymerase (RdRp) phylogeny revealed that all of these viruses cluster in two readily distinguishable groups (37–39), i.e., clade 1 (Cruliviridae, Fimoviridae, Hantaviridae, Peribunyaviridae, Phasmaviridae, Tospoviridae, and Tulasviridae) and clade 2 (Arenaviridae, Discoviridae, Leishbuviridae, Mypoviridae, Nairoviridae, Phenuiviridae, and Wupedeviridae). In April 2024, the ICTV approved taxonomic proposal (TaxoProp) 2023.024M.Bunyaviricetes (40), resulting in class Ellioviricetes being renamed Bunyaviricetes (Fig. 1); order Bunyavirales being renamed Elliovirales and all clade 2 taxa removed from this order; and establishment of a new order, Hareavirales (from Basque harea, meaning sand; a reference to Arenaviridae and sandfly-borne viruses of Phenuiviridae), for all clade 2 taxa. In addition, a new family, Konkoviridae, was established and included in order Hareavirales [TaxoProps 2023.006M.Bunyavirales_1nfam_1ngen_1nsp and 2023.006MX.Bunyavirales_1nfam_1ngen_1nsp_Error_Correction (40)] (Fig. 2). The decision to change the name of class Ellioviricetes to Bunyaviricetes was made to ensure that the word stem “bunya” remains applicable to all viruses of the original five genera established in former family Bunyaviridae.

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).

Bunyaviricete diversity

Classification of viruses by the ICTV is dependent on the submission of TaxoProps by the virology community and succeeds only by meeting specific rigorous standards, including the now-mandatory requirement of coding-complete virus genome sequences (42). Alas, many viruses that appear to be obvious bunyaviricetes remain unclassified because suitable proposals have not been prepared and submitted. The number of classified bunyaviricetes pales in comparison to the number of known related RdRp sequences in GenBank and sequence read archives; these RdRp sequences represent viruses but by themselves do not suffice for official classification. However, they can be used to establish phylogenetic trees, thereby providing a glimpse into the future of bunyaviricete classification. A cursory examination of such trees reveals that, for instance, fungal, invertebrate, plant, and stramenopile bunyaviricete diversity is likely enormous, but many of these viruses could likely be accommodated within the established two orders. Indeed, the Halophytophthora RNA virus 8 RdRp and its relatives form an obvious ellioviral family ‘Epsilonmycobunyaviridae’ (29), and the recently suggested ‘Rhizoctobunyaviridae’ (43) should be absorbed in ellioviral family Tulasviridae adjacent to a new tentative family ‘Sclerobunyaviridae’ (44). Order Hareavirales may be expanded in the future by tentative families ‘Gammaymycobunyaviridae’ (45) and ‘Zetamycobunyaviridae’ (46–49).

Many deposited RdRp sequences already portend challenges to the current classification. For instance, the Botrytis cinerea negative-stranded RNA virus 1 and Macrophomina phaseolina negative-stranded RNA virus 1 RdRps and their numerous immediate relatives (29, 50) together with a sister clade of lower plant virus RdRps (33) could represent tentatively named ellioviral families ‘Deltamycobunyaviridae’ and ‘Viridisbunyaviridae’ but may also be considered a third bunyaviricete order to include many families. However, coding-complete genome sequences are not available for most of these viruses and hence they may not be classified (42, 51). In fact, in many cases, not even nucleocapsid-encoding sequences have been uncovered in conjunction with the RdRp-encoding sequences. These nucleocapsid-encoding sequences may be too divergent from known sequences to be readily identified. Alternatively, some of these viruses may have acquired alternative structural protein genes and/or evolved capsidless lifestyles. In the latter case, deep phylogenetic analysis will have to be performed to determine whether these entities can still be considered (derived) viruses as per the current ICTV-adopted virus definition (51, 52) or whether they constitute non-viral mobile genetic elements related to viruses.

Other imminent challenges include determining the taxonomic position of the family Tosoviridae and class Insthoviricetes (families Amnoonviridae and Orthomyxoviridae). Family Tosoviridae was established in 2023 (22, 53) for a single virus, turtle fraservirus 1 (TFV1; species Fraservirus testudinis), isolated from diseased freshwater turtles (54). At the time of discovery, the TFV1 RdRp was not assignable to either of the two negarnaviricot subphyla (Haploviricotina or Polyploviricotina) and hence this family is currently “free-floating” in the phylum (22). In the same analysis, class Insthoviricetes clustered separately from all bunya-like viruses but within Polyploviricotina (54) (Fig. 3). Analyses performed with the now newly increased RdRp sequence data set indicate that both Tosoviridae and Insthoviricetes may have to be absorbed by Bunyaviricetes (Y. I. Wolf., unpublished data). However, whereas TFV1 at least resembles hareaviral arenavirids in the genomic organization, insthoviricetes appear to be highly dissimilar from classified bunyaviricetes. Additional phylogenetic and structural analyses of non-RdRp proteins encoded by bunyaviricetes and insthoviricetes may clarify this issue and should be encouraged (along with submission of TaxoProps) to assist in further improving polyploviricotine taxonomy.

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).

The views expressed in this article do not necessarily reflect the views of the journal or of ASM.

ETHICS APPROVAL

This work did not include any work with humans or animals.