# ICTV Virus Taxonomy Profile: Amnoonviridae 2023

Eugene V Koonin, Mart Krupovic, Win Surachtpong, Yuri I Wolf, Jens H Kuhn

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► To cite this version:

Eugene V Koonin, Mart Krupovic, Win Surachtpong, Yuri I Wolf, Jens H Kuhn. ICTV Virus Taxonomy Profile: Amnoonviridae 2023. Journal of General Virology, 2023, 104 (10), pp.001903. 10.1099/jgv.0.001903. pasteur-04313778

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Submitted on 29 Nov 2023

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# ICTV Virus Taxonomy Profile: Amnoonviridae 2023

Eugene V. Koonin¹, Mart Krupovic², Win Surachtpong³, Yuri I. Wolf¹ and Jens H. Kuhn⁴*

## Abstract

*Amnoonviridae* is a family of negative-sense RNA viruses with genomes totalling about 10.3 kb. These viruses have been found in fish. The amnoonvirid genome consists of 10 segments, each with at least 1 open reading frame (ORF). The RNA1-3 ORFs encode the three subunits of the viral polymerase. The RNA4 ORF encodes a nucleoprotein. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the family *Amnoonviridae*, which is available at **ictv.global/report/amnoonviridae**.

<table><caption>**Table 1.** Characteristics of members of the family *Amnoonviridae*</caption><thead><tr><td>Example</td><td>tilapia lake virus (KU751814–KU751823), species <i>Tilapinevirus tilapiae</i>, genus <i>Tilapinevirus</i></td></tr></thead><tbody><tr><td>Virion</td><td>Enveloped, spherical; 55–100 nm</td></tr><tr><td>Genome</td><td>About 10.3 kb of decasegmented negative-sense RNA</td></tr><tr><td>Replication</td><td>Unknown</td></tr><tr><td>Translation</td><td>Unknown</td></tr><tr><td>Host range</td><td>Actinopterygiid fish</td></tr><tr><td>Taxonomy</td><td>Realm <i>Riboviria</i>, kingdom <i>Orthornavirae</i>, phylum <i>Negarnaviricota</i>, class <i>Insthoviricetes</i>, order <i>Articulavirales</i>; the family includes the genus <i>Tilapinevirus</i> and the species <i>Tilapinevirus tilapiae</i></td></tr></tbody></table>

## VIRION

Amnoonvirids produce spherical, slightly pleomorphic (likely enveloped) particles 55–100 nm in diameter [1, 2] (Table 1).

## GENOME

The amnoonvirid genome comprises 10 segments of linear negative-sense RNA with a total length of about 10.3 kb (tilapia lake virus – RNA1:1641 nt; RNA2:1471 nt; RNA3:1371 nt; RNA4:1250 nt; RNA5:1099 nt; RNA6:1044 nt; RNA7:777 nt; RNA8:657 nt; RNA9:548 nt; and RNA10:465 nt) (Fig. 1). All 10 segments have conserved,

complementary sequences at their 5'- and 3'-ends. The RNA1 ORF encodes a protein with an RNA-directed RNA polymerase (RdRP) domain homologous to the PB1 of influenza C virus (*Orthomyxoviridae: Gammainfluenza-virus*) [3–5]. The RNA2 and RNA3 ORFs encode the PB2 and PA polymerase subunit homologues of orthomyxovirids [6]. The RNA4 ORF encodes a nucleoprotein [7].

## REPLICATION

Cell entry occurs via dynamin-mediated endocytosis in a cholesterol-dependent, cytoskeleton-dependent manner that is independent of clathrin and pH [8].

Received 25 September 2023; Accepted 26 September 2023; Published 24 October 2023

**Author affiliations:** ¹National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda MD 20894, USA; ²Institut Pasteur, Université Paris Cité, Archaeal Virology Unit, Paris 75015, France; ³Department of Veterinary Microbiology and Immunology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand; ⁴Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, MD 21702, USA.

*Correspondence: Jens H. Kuhn, kuhnjens@mail.nih.gov

Keywords: ICTV Report; taxonomy; *Amnoonviridae*; tilapinevirus; tilapia lake virus.

Abbreviations: NP, nucleoprotein; RdRP, RNA-directed RNA polymerase.

001903

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<figure><img src="image_7.png" /><figcaption>**Fig. 1.** Genome organisation of tilapia lake virus. ORFs are coloured 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 coloured grey.</figcaption></figure>

<figure><img src="image_8.png" /><figcaption>**Fig. 2.** Phylogenetic relationships of the RdRP core domain of viruses in the phylum *Negarnaviricota*. For full details see *Amnoonviridae* ICTV Report.</figcaption></figure>

## References

1. Eyngor M, Zamostiano R, Kembou Tsofack JE, Berkowitz A, Bercovier H, et al. Identification of a novel RNA virus lethal to tilapia. *J Clin Microbiol* 2014;52:4137–4146.

2. Del-Pozo J, Mishra N, Kabuusu R, Cheetham S, Eldar A, et al. Syncytial hepatitis of tilapia (*Oreochromis niloticus* L.) is associated with orthomyxovirus-like virions in hepatocytes. *Vet Pathol* 2017;54:164–170.

3. Ortiz-Baez AS, Eden JS, Moritz C, Holmes EC. A divergent *Articula-virus* in an Australian gecko identified using meta-transcriptomics and protein structure comparisons. *Viruses* 2020;12:613.

## PATHOGENICITY

Tilapia lake virus is highly virulent in tilapia, with systemic infection involving most organs. Infection results in lethargy, ocular disease (such as cataracts, endophthalmitis or exophthalmos), skin erosions and haemorrhages, and severe anaemia, leading to death in >80% of cases [1].

## TAXONOMY

Current taxonomy: **ictv.global/taxonomy**. The family *Amnoonviridae* includes the genus *Tilapinevirus* for one species of viruses that infect fish. Viruses in the family *Amnoonviridae* are most closely related to articulaviral orthomyxovirids [4] (Fig. 2).

## RESOURCES

Full ICTV Report on the family *Amnoonviridae*: **ictv.global/report/amnoonviridae**.

### Funding information

Production of this Profile, the ICTV Report, and associated resources was supported by the Microbiology Society. This work was supported in part through the Laulima Government Solutions, LLC, prime contract with the US National Institute of Allergy and Infectious Diseases (NIAID), under contract no. HHSN272201800013C. J.H.K. performed this work as an employee of Tunnell Government Services (TGS), a subcontractor of Laulima Government Solutions, LLC, under contract no. HHSN272201800013C. The content of this publication should not be interpreted as necessarily representing the official policies, either expressed or implied, of the US Department of Health and Human Services or of the institutions and companies affiliated with the authors.

### Acknowledgements

We thank Stuart G. Siddell, Elliot J. Lefkowitz, Sead Sabanadzovic, Peter Simmonds, F. Murilo Zerbini, Evelien Adriaenssens, Luisa Rubino, Arvind Varsani (ICTV Report Editors), and Donald B. Smith (Managing Editor, ICTV Report). We thank Anya Crane (Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, MD, USA) for critically editing the manuscript.

### Conflicts of interest

The authors declare that there are no conflicts of interest.

4. Bacharach E, Mishra N, Briese T, Zody MC, Kembou Tsofack JE, et al. Characterization of a novel orthomyxo-like virus causing mass die-offs of tilapia. *mBio* 2016;7:e00431–16.

5. Acharya V, Chakraborty HJ, Rout AK, Balabantaray S, Behera BK, et al. Structural characterization of open reading frame-encoded functional genes from tilapia lake virus (TiLV). *Mol Biotechnol* 2019;61:945–957.

6. Arragain B, Pelosse M, Thompson A, Cusack S. Structural and functional analysis of the minimal orthomyxovirus-like polymerase of tilapia lake virus from the highly diverged *Amnoonviridae* family. *bioRxiv* 2023;553164;2023.

7. Abu Rass R, Kustin T, Zamostiano R, Smorodinsky N, Ben Meir D, et al. Inferring protein function in an emerging virus: detection of the nucleoprotein in tilapia lake virus. *J Virol* 2022;96:e0175721.

8. Abu Rass R, Kembou-Ringert J-E, Zamostiano R, Eldar A, Ehrlich M, et al. Mapping of tilapia lake virus entry pathways with inhibitors reveals dependence on dynamin activity and cholesterol but not endosomal acidification. *Front Cell Dev Biol* 2022;10:1075364.