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Hartmaan Institute snake virus 1 (HISV-1) is the only currently classified hartmanivirus. Like reptarenaviruses, but unlike antennaviruses and mammarenaviruses, hartmaniviruses infect captive snakes. In contrast to mammarenaviruses and reptarenaviruses, but similar to antennaviruses, hartmaniviruses lack the gene encoding the zinc finger matrix protein (Z) (Hepojoki et al., 2018).
Virions are spherical or pleomorphic in shape, 120–150 nm in diameter, with dense lipid envelopes (Figure 1.Hartmanivirus). The virion surface layer is covered with club-shaped projections. These projections are made of trimeric spike structures of two virus-encoded membrane glycoprotein (GP) subunits (GP1 and GP2) and a stable signal peptide (SSP) (Hepojoki et al., 2018).
Figure 1.Hartmanivirus. Hartmanivirus particles. A) Cryo-electron micrograph of HISV-1. Courtesy of Pasi Laurinmäki and Sarah Butcher, Cryo-EM Core Facility, Biocenter Finland, University of Helsinki, Finland. B) Negative-stain electron micrograph of HISV-1. Courtesy of Andrea Laimbacher and Elisabeth M. Schraner, Institute of Veterinary Anatomy and Virology, Vetsuisse Faculty, University of Zurich, Switzerland.
Virions contain 1 ambisense and 1 negative-sense single-stranded RNA segment that are encapsidated independently. The termini of the RNAs contain inverted complementary sequences encoding transcription and replication initiation signals (Hepojoki et al., 2018).
Viruses express 3 structural proteins. The most abundant structural protein in virions is nucleoprotein (NP), which encapsidates the genomic segments. The least abundant protein is the RNA-dependent RNA polymerase (L), which mediates virus genome replication and transcription. Glycoproteins (GP1 and GP2) are derived by post-translational cleavage from an intracellular glycoprotein precursor, GPC. A third GPC cleavage product, the stable signal peptide (SSP), stays attached to the GP complex (Hepojoki et al., 2018).
Not reported. SSP is likely myristoylated (Hepojoki et al., 2018).
The S RNA of hartmaniviruses encodes two proteins in non-overlapping open reading frames (ORFs) of opposite polarities (ambisense coding arrangement) that are separated by non-coding intergenic regions (IGRs) (Figure 2.Hartmanivirus): NP in the virus genome-complementary sequence, and GPC in the virus genome-sense sequence. The L RNA encodes L in the virus genome-complementary sequence. The IGR forms one or more energetically stable stem-loop (hairpin) structures and functions in structure-dependent transcription termination and in virion assembly and budding (Hepojoki et al., 2018).
Figure 2.Hartmanivirus. Schematic representation of the bisegmented hartmanivirus genome organization. The 5'-and 3'-ends of both segments (S and L) are complementary at their termini, likely promoting the formation of circular ribonucleoprotein complexes within the virion. GPC, glycoprotein precursor; L, RNA-dependent RNA polymerase; NP, nucleoprotein. Intergenic regions (IGRs), which form hairpin structures (not shown), separate open reading frames.
Hartmaniviruses were first discovered in Helsinki, Finland, in a captive German boa constrictor (Squamata: Boidae: Boa constrictor Linnaeus, 1758) that was co-infected with a reptarenavirus and had boid inclusion body disease (BIBD) (Hepojoki et al., 2015). Several distinct hartmaniviruses were since isolated in boa constrictor I/1Ki cells. Whether hartmaniviruses cause disease in snakes remains to be determined (Hepojoki et al., 2018).
Exemplar isolate of the speciesSpeciesVirus nameIsolateAccession numberRefSeq numberAvailable sequenceVirus Abbrev.Haartman hartmanivirusHaartman Institute snake virus 11L: KR870031; S: KR870017L: NC_043443; S: NC_043444Complete coding genomeHISV-1Muikkunen hartmanivirusDante Muikkunen virus 1F18-5L: MH778629; S: MH483026Complete coding genomeDaMV-1Schoolhouse hartmanivirusold schoolhouse virus 1F17-0012-1 and -3L: MH483025; S: MH483024Complete coding genomeOScV-1Zurich hartmanivirusveterinary pathology Zurich virus 1S14-369 to -79 poolL: MH483032; S: MH483031Complete coding genomeVPZV-1
Hartmanivirus: from Haartman Institute, located at the University of Helsinki in Finland, the place where HISV-1 was first discovered (Hepojoki et al., 2015).
Phylogenetic relationships across the genus have been established from maximum likelihood trees generated from complete of NP and L proteins (Figure 3.Hartmanivirus).
Figure 3.Hartmanivirus. Maximum likelihood phylogenetic trees inferred from PRANK alignments (Löytynoja and Goldman 2008) of the complete NP (A: top) and L (B: bottom) amino acid sequences. For both alignments, the best-fit model of protein evolution (LG+G) was selected using ProtTest 3 (v. 3.4.2) (Darriba et al., 2011). Maximum likelihood trees with 1,000 bootstrap replicates were produced using RAxML (v. 8) (Stamatakis 2014). The percentage of replicate trees in which the associated taxa clustered together in the bootstrap is shown next to branch nodes (when ≥ 70%). The mid-point rooted trees were visualized using FigTree (http://tree.bio.ed.ac.uk/). For both NP and L, the sequence of Haartman Institute snake virus 1 (red dots) and 6 unclassified hartmaniviruses (white dots) were included. In both trees, representative viruses of the genera Mammarenavirus and Reptarenavirus are also included (green and yellow dots).
Dante Muikkunen virus 1
S segment: MH483026; Lsegment: MH778629
Haartman Institute snake virus 2
S segment: MH483041; Lsegment: MH483042
old schoolhouse virus 1
S segment: MH483024; Lsegment: MH483025
old schoolhouse virus 2
S segment: MH483029; Lsegment: MH483030
veterinary pathology Zurich virus 1
S segment: MH483031; Lsegment: MH483032
veterinary pathology Zurich virus 2
S segment: MH483043; Lsegment: MH483044
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