Taxonomic reorganization of the family Bornaviridae

Abstract

Knowledge of bornaviruses has expanded considerably during the last decade. A possible reservoir of mammalian Borna disease virus has been identified, divergent bornaviruses have been detected in birds and reptiles, and endogenous bornavirus-like elements have been discovered in the genomes of vertebrates of several species. Previous sequence comparisons and alignments have indicated that the members of the current family Bornaviridae are phylogenetically diverse and are not adequately classified in the existing bornavirus taxonomy supported by the International Committee on Taxonomy of Viruses (ICTV). We provide an update of these analyses and describe their implications for taxonomy. We propose retaining the family name Bornaviridae and the genus Bornavirus but reorganizing species classification. PAirwise Sequence Comparison (PASC) of bornavirus genomes and Basic Local Alignment Search Tool (BLAST) comparison of genomic and protein sequences, in combination with other already published phylogenetic analyses and known biological characteristics of bornaviruses, indicate that this genus should include at least five species: Mammalian 1 bornavirus (classical Borna disease virus and divergent Borna disease virus isolate No/98), Psittaciform 1 bornavirus (avian/psittacine bornaviruses 1, 2, 3, 4, 7), Passeriform 1 bornavirus (avian/canary bornaviruses C1, C2, C3, LS), Passeriform 2 bornavirus (estrildid finch bornavirus EF), and Waterbird 1 bornavirus (avian bornavirus 062CG). This classification is also in line with biological characteristics of these viruses and their vertebrate hosts. A snake bornavirus, proposed to be named Loveridge's garter snake virus 1, should be classified as a member of an additional species (Elapid 1 bornavirus), unassigned to a genus, in the family Bornaviridae. Avian bornaviruses 5, 6, MALL, and another "reptile bornavirus" ("Gaboon viper virus") should stay unclassified until further information becomes available. Finally, we propose new virus names and abbreviations when necessary to achieve clear differentiation and unique identification.

Fig. 1

Distribution of pairwise identities among complete sequences of 16 viruses in the family Bornaviridae. The NCBI PASC alignment tool automatically assigns peak colors (brown, green) based on NCBI virus taxonomy. Regions represent genome pairs belonging to the same species (A) and to different species but to the same genus (B), respectively. Since most of the sequences used for PASC analysis are currently not classified in NCBI taxonomy the same way as proposed in this paper, the colors in this screenshot do not follow the grouping, thereby visually demonstrating that the current bornavirus taxonomy is ill-advised. For instance, bornavirus genomes EU781967 and FJ620690 are 97% identical and therefore should belong to the same species in one genus. However, in the current NCBI taxonomy, EU781967 is assigned to the species Borna disease virus in the genus Bornavirus, whereas FJ620690 is assigned to an unclassified species in an unclassified genus in the family Bornaviridae. Therefore, since the NCBI taxonomy tool does not assign both sequences to the same species or the same genus, the bar at 97% in the current PASC figure is colored brown rather than green. X-axis, percentage of identity; y-axis, number of genome pairs

Fig. 2

The same distribution of pairwise identities among complete sequences of 16 viruses in the family Bornaviridae as in Figure 1, but colored as if the taxonomy proposed in this manuscript was accepted by the ICTV and then adopted by NCBI. Peaks above 75% identity (region A, green) represent genome pairs belonging to the same species. Peaks between 60 and 71% identity (region B, yellow) represent genome pairs belonging to different species but the same genus. Peaks below 60% identity (region C, brown) represent genome pairs that belong to a separate genus (not yet proposed in this manuscript). X-axis, percentage of identity; y-axis, number of genome pairs

Fig. 3

Phylogenetic tree of a 1824-nt stretch of 17 selected nucleic acid sequences coding for N, X, and P proteins and the N/X intergenic region of bornaviruses. Phylogenetic neighbor-joining analysis was conducted using the MEGA5 program [55]. The evolutionary distances were computed using the Kimura 2-parameter model. Bootstrap resampling analysis with 1,000 replicates was employed; percentages ≥60% are shown next to the branches.

Fig. 4

Phylogenetic tree of 15 selected amino acid sequences representing the X protein of bornaviruses. Phylogenetic neighbor-joining analysis was conducted using the MEGA5 program [55]. The evolutionary distances were computed using the p-distance method. Bootstrap resampling analysis with 1,000 replicates was employed; percentages ≥60% are shown next to the branches.