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• Family: Amnoonviridae
  • Genus: Tilapinevirus
• Authors: Amnoonviridae
• Citation: Amnoonviridae
• References: Amnoonviridae
• Resources: Amnoonviridae
• Species List: Amnoonviridae

Family:Amnoonviridae

Eugene V. Koonin, Mart Krupovic, Win Surachetpong (วินสุรเชษฐพงษ์), Yuri I. Wolf, and Jens H. Kuhn

The citation for this ICTV Report chapter is the summary published as:

Koonin, E. V., Krupovic, M., Surachetpong, W., Wolf, Y. I., & Kuhn, J. H., (2023): ICTV Virus Taxonomy Profile:Amnoonviridae2023, Journal of General Virology 104, 001903

Corresponding author: Jens H. Kuhn (kuhnjens@mail.nih.gov)
Edited by:Jens H. Kuhn and Stuart G. Siddell
Posted: September 2023

Summary

Amnoonviridaeis a family of negative-sense RNA viruses with genomes totaling about 10.3 kb (Table 1.Amnoonviridae). These viruses have been found in actinopterygiid fish (in particular tilapia) and squamate reptiles (Gulf tree gehyras) sampled in Africa, Asia, and North America. The family includes a single genus with one species for one virus. The amnoonvirid genome consists of 10 segments, each with at least one open reading frame (ORF). The RNA1–3 ORFs encode the three subunits of the viral polymerase. The RNA4 ORF encodes a nucleoprotein.

Table 1.Amnoonviridae Characteristics of members of the familyAmnoonviridae

Virion

Morphology

Amnoonvirids produce spherical, slightly pleomorphic and likely enveloped particles that are 55–100 nm in diameter (Eyngoret al., 2014,Del-Pozoet al., 2017).

Nucleic acid

Amnoonvirids have 10 segments of linear negative-sense RNA with a total length of about 10.3 kb (tilapia lake virus - RNA1: 1,641 nt; RNA2: 1,471 nt; RNA3: 1,371 nt; RNA4: 1,250 nt; RNA5: 1,099 nt; RNA6: 1,044 nt; RNA7: 777 nt; RNA8: 657 nt; RNA9: 548 nt; and RNA10: 465 nt (Bacharachet al., 2016).

Genome organization and replication

Viruses of the familyAmnoonviridae have deca-segmented genomes, with each segment possessing one primary ORF (Figure 1.Amnoonviridae). The RNA1 ORF encodes a protein with an RNA-directed RNA polymerase (RdRP) domain homologous to influenza C virus (Orthomyxoviridae:Gammainfluenzavirus) PB1 (Bacharachet al., 2016,Acharyaet al., 2019,Ortiz-Baezet al., 2020). The RNA2 and RNA3 ORFs encode the PB2 and PA polymerase subunit homologs of orthomyxovirids (Arragainet al., 2023). The RNA4 ORF encodes a nucleoprotein (Abu Rasset al., 2022b). The identities and functions of proteins encoded by the remaining segments are unknown. The replication cycle of amnoonvirids remains to be determined. All 10 segments have conserved, complementary sequences at their 5′- and 3′-ends, similar to segment termini found in orthomyxovirid genome sequences (Bacharachet al., 2016). In contrast to orthomyxovirids, amnoonvirids do not hemagglutinate red blood cells, suggesting that they enter host cells differently (Chengulaet al., 2019). However, entry occurs via dynamin-mediated endocytosis in a cholesterol-dependent, cytoskeleton-dependent manner that is independent of clathrin and pH (Abu Rasset al., 2022a).

Figure 1.Amnoonviridae.Genome length, organization, and position of open reading frames (ORFs) of tilapia lake virus, the only classified virus in the familyAmnoonviridae, ORFs are indicated as boxes, colored according to the predicted protein function (NP, nucleoprotein gene;PA; polymerase subunit 3 gene;PB1, polymerase subunit 1 gene encoding an RdRP domain;PB2, polymerase subunit 2 gene). Genes of unknown function are colored gray.

Biology

The only classified amnoonvirid, tilapia lake virus (TiLV), has been detected in sick and deceased wild and farmed Nile tilapia (cichlidOreochromis niloticus (Linnaeus, 1758)), Nile tilapia x blue tilapia (Oreochromis aureus (Steindachner, 1864)) hybrids, and Mozambique tilapia (Oreochromis mossambicus (W. K. H. Peters, 1852)) in Bangladesh (Debnathet al., 2020), China/Taiwan (World Organisation for Animal Health 2023), Colombia (Contreraset al., 2021), Ecuador (Bacharachet al., 2016), Egypt (Nicholsonet al., 2017), India (Swaminathanet al., 2021), Israel (Bacharachet al., 2016), Kenya (Mugimbaet al., 2018), Malaysia (World Organisation for Animal Health 2023), Mexico (World Organisation for Animal Health 2023), Peru (World Organisation for Animal Health 2023), Philippines (World Organisation for Animal Health 2023), Tanzania (Mugimbaet al., 2018), Thailand (Surachetponget al., 2017), Uganda (Mugimbaet al., 2018), United States (Ahasanet al., 2020), and Viet Nam (Tranet al., 2022). TiLV has also been found in apparently healthy giant gourami (osphronemidOsphronemus goramy Lacépède, 1801) sampled in Thailand (Chiamkunakornet al., 2019).

Unclassified amnoonvirids have been found in diverse actinopterygiid fish (Turnbullet al., 2020,Li 2023), with the exception of Lauta virus, which was discovered in Gulf tree gehyras (gekkonidGehyra lauta Oliver, Prasetya, Tedeschi, Fenker, Ellis, Doughty, & Moritz, 2020) sampled in Australia (Ortiz-Baezet al., 2020).

TiLV causes a systemic disease involving most organs, with virus present also in muscles, mucus, and feces (Eyngoret al., 2014,Bacharachet al., 2016,Tattiyaponget al., 2018,Mugimbaet al., 2019,Yamkasemet al., 2021b). Infection results in lethargy, ocular disease (such as, cataracts, endophthalmitis or exophthalmos), skin erosions and hemorrhages, and severe anemia, leading to death in >80% of cases (Eyngoret al., 2014,Tattiyaponget al., 2017,Turneret al., 2023). TiLV is also virulent in experimentally exposed larval and adult zebrafish (cyprinidDanio rerio (F. Hamilton, 1822)) (Rakuset al., 2020,Widzioleket al., 2021), Malawi cichlids (Aulonacara spp.) (Yamkasemet al., 2021a), and Mozambique tilapia (Oreochromis mossambicus (W. K. H. Peters, 1852)) (Waiyamitraet al., 2021), and replicates subclinically in firemouth cichlids (Thorichthys meeki Brind, 1918) and freshwater angelfish (cichlidPterophyllum scalare (Schultze, 1823)) (Pariaet al., 2023). Experimentally, TiLV can infect and cause mass mortality in red tilapia and giant gourami, but does not infect Asian sea bass (latidLates calcarifer (Bloch, 1790)), climbing perch (anabantidAnabas testudineus (Bloch, 1792)), common carp (cyprinidCyprinus carpio Linnaeus, 1758), goldfish (cyprinidCarassius auratus (Linnaeus, 1758)), iridescent sharks (pangasiidPangasianodon hypophthalmus (Sauvage, 1878)), parrotfish (cichlidAmphilophus citrinellus (Günther, 1864) xVieja melanurus (Günther, 1862)), silver barb (cyprinid Barbodes gonionotus (Bleeker, 1850)), snakeskin gouramis (osphronemidTrichogaster pectoralis Regan, 1910), striped snake-head fish (channid Channa striata (Bloch, 1793)), three spot gourami (osphronemidTrichopodus trichopterus (Pallas, 1770)), or walking catfish (clariidClarias macrocephalus Günther, 1864) (Jaemwimolet al., 2018,Pariaet al., 2023).

Derivation of names

Amnoonviridae: from Hebrew אַמְנוּן [amnun/amnoon] for tilapia

tilapiae: fromtilapia

Tilapinevirus: from the adjectivetilapine, referring to fish of tribe Tilap(i)ini

Genus demarcation criteria

Not applicable (the family includes only a single genus).

Species demarcation criteria

Not applicable (the only genus includes only a single species).

Relationships within the family

Phylogenetic relationships of TiLV to members of the phylumNegarnaviricota are shown in Figure 2.Amnoonviridae.

Figure 2.Amnoonviridae. Phylogenetic relationships of TiLV to members of the phylumNegarnaviricota. The list of complete exemplar genomes ofNegarnaviricota was obtained from the ICTV Virus Metadata Resource (VMR) datasheet v.38.1 (https://ictv.global/vmr). RdRP core domains were identified by running a PSI-BLAST search against either the protein coding gene complement or six-frame translation of the virus RNA sequences using the 143 negarnaviricot profiles (Neriet al., 2022) and a tosovirid profile (Waltzeket al., 2022). RdRP core fragments were clustered using MMSEQS2 with the sequence similarity threshold of 0.3; sequences in each cluster were aligned using MUSCLE5. A consensus sequence was derived from each alignment; consensus sequences were aligned using MUSCLE5, then each consensus amino acid was expanded into an alignment column (Neriet al., 2022). An approximate ML phylogenetic tree was reconstructed from this alignment of 1122 negarnaviricot RdRP core sequences using FastTree (WAG evolutionary model, gamma-distributed site rates). A representative sequence (one, closest to the family root) was selected for each of the 36 negarnaviricot families and the full tree was trimmed to these 36 representative leaves.

Relationships with other taxa

Viruses in the familyAmnoonviridae are most closely related to articulaviral orthomyxovirids (Bacharachet al., 2016).

Related, unclassified viruses

Virus names and virus abbreviations are not official ICTV designations.

* Incomplete genome