1887

Abstract

Over the last decade, a number of USA aquaculture facilities have experienced periodic mortality events of unknown aetiology in their clownfish (). Clinical signs of affected individuals included lethargy, altered body coloration, reduced body condition, tachypnea, and abnormal positioning in the water column. Samples from outbreaks were processed for routine parasitological, bacteriological, and virological diagnostic testing, but no consistent parasitic or bacterial infections were observed. Histopathological evaluation revealed individual cell necrosis and mononuclear cell inflammation in the branchial cavity, pharynx, esophagus and/or stomach of four examined clownfish, and large basophilic inclusions within the pharyngeal mucosal epithelium of one fish. Homogenates from pooled external and internal tissues from these outbreaks were inoculated onto striped snakehead (SSN-1) cells for virus isolation and cytopathic effects were observed, resulting in monolayer lysis in the initial inoculation and upon repassage. Transmission electron microscopy of infected SSN-1 cells revealed small round particles (mean diameter=20.0–21.7 nm) within the cytoplasm, consistent with the ultrastructure of a picornavirus. Full-genome sequencing of the purified virus revealed a novel picornavirus most closely related to the bluegill picornavirus and other members of the genus . Additionally, pairwise protein alignments between the clownfish picornavirus (CFPV) and other known members of the genus yielded results in accordance with the current International Committee on Taxonomy of Viruses criteria for members of the same genus. Thus, CFPV represents a proposed new limnipivirus species. Future experimental challenge studies are needed to determine the role of CFPV in disease.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001421
2020-05-18
2020-06-04
Loading full text...

Full text loading...

/deliver/fulltext/jgv/10.1099/jgv.0.001421/jgv001421.html?itemId=/content/journal/jgv/10.1099/jgv.0.001421&mimeType=html&fmt=ahah

References

  1. Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ et al. ICTV Virus Taxonomy Profile: Picornaviridae. J Gen Virol 2017; 98:2421–2422 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  2. King AMQ, Lefkowitz EJ, Mushegian AR, Adams MJ, Dutilh BE et al. Changes to taxonomy and the International Code of virus classification and nomenclature ratified by the International Committee on taxonomy of viruses (2018). Arch Virol 2018; 163:2601–2631 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  3. Racaniello VP. Picornaviridae: The viruses and their replication. In Knipe DM, Howley PM. (editors) Fields Virology, 6th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2013 pp 453–489
    [Google Scholar]
  4. Jiang P, Liu Y, Ma H-C, Paul AV, Wimmer E. Picornavirus morphogenesis. Microbiol Mol Biol Rev 2014; 78:418–437 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  5. Woo PCY, Lau SKP, Choi GKY, Huang Y, Teng JLL et al. Natural occurrence and characterization of two internal ribosome entry site elements in a novel virus, canine picodicistrovirus, in the picornavirus-like superfamily. J Virol 2012; 86:2797–2808 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  6. Reuter G, Boros Ákos, Földvári G, Szekeres S, Mátics R et al. Dicipivirus (family Picornaviridae) in wild Northern white-breasted hedgehog (Erinaceus roumanicus). Arch Virol 2018; 163:175–181 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  7. Lin J-Y, Chen T-C, Weng K-F, Chang S-C, Chen L-L et al. Viral and host proteins involved in picornavirus life cycle. J Biomed Sci 2009; 16:103 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  8. TFF N. Personal observation; 2019
  9. Moore AR, LI MF, McMENEMY M. Isolation of a picorna-like virus from smelt, Osmerus mordax (Mitchill). J Fish Dis 1988; 11:179–184 [CrossRef]
    [Google Scholar]
  10. Ahne W, Anders K, Halder M, Yoshimizu M. Isolation of picornavirus-like particles from the European smelt, Osmerus eperlanus (L.). J Fish Dis 1990; 13:167–168 [CrossRef]
    [Google Scholar]
  11. Hedrick RP, McDowell TS, Kent ML, Elston RA. A small RNA virus isolated from Atlantic salmon (Salmo salar). J Appl Ichthyol 1990; 6:173–181 [CrossRef]
    [Google Scholar]
  12. Hedrick RP, Yun S, Wingfield WH. A small RNA virus isolated from salmonid fishes in California, USA. Can J Fish Aquat Sci 1991; 48:99–104 [CrossRef]
    [Google Scholar]
  13. Eaton WD, Bagshaw J, Hulett J, Evans S. Isolation of a picorna-like virus from steelhead in Washington state. J Aquat Anim Health 1992; 4:90–96 [CrossRef]
    [Google Scholar]
  14. Glazebrook JS, Heasman MP, BEER SW. Picorna-like viral particles associated with mass mortalities in larval barramundi, Lates calcarifer Bloch. J Fish Dis 1990; 13:245–249 [CrossRef]
    [Google Scholar]
  15. Munday BL, Langdon JS, Hyatt A, Humphrey JD. Mass mortality associated with a viral-induced vacuolating encephalopathy and retinopathy of larval and juvenile barramundi, Lates calcarifer Bloch. Aquaculture 1992; 103:197–211 [CrossRef]
    [Google Scholar]
  16. Bloch B, Gravningen K, Larsen JL. Encephalomyelitis among turbot associated with a picornavirus-like agent. Dis Aquat Organ 1991; 10:65–70 [CrossRef]
    [Google Scholar]
  17. Breuil G, Bonami JR, Pepin JF, Pichot Y. Viral infection (picorna-like virus) associated with mass mortalities in hatchery-reared sea-bass (Dicentrarchus labrax) larvae and juveniles. Aquaculture 1991; 97:109–116 [CrossRef]
    [Google Scholar]
  18. Mori K-ichiro, Nakai T, Nagahara M, Muroga K, Mekuchi T et al. A viral disease in hatchery-reared larvae and juveniles of redspotted grouper. Fish Pathol 1991; 26:209–210 [CrossRef]
    [Google Scholar]
  19. Iwanowicz LR, Goodwin AE, Heil N. A small RNA virus isolated from apparently healthy wild sandbar shiners, Notropis scepticus (Jordan & Gilbert). J Fish Dis 2000; 23:349–352 [CrossRef]
    [Google Scholar]
  20. Petty BD, Fraser WA. Viruses of PET fish. Vet Clin North Am Exot Anim Pract 2005; 8:67–84 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  21. Reuter G, Pankovics P, Delwart E, Boros Ákos. A novel posavirus-related single-stranded RNA virus from fish (Cyprinus carpio). Arch Virol 2015; 160:565–568 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  22. Batts W, Yun S, Hedrick R, Winton J. A novel member of the family Hepeviridae from cutthroat trout (Oncorhynchus clarkii). Virus Res 2011; 158:116–123 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  23. Bovo G, Florio D. Viral diseases of cultured marine fish. In Eiras JC, Segner H, Wahli T, Kapoor BG. (editors) Fish Diseases, 1st ed. Science Publishers: Enfield, NH; 2008 pp 185–238
    [Google Scholar]
  24. Walker PJ, Winton JR. Emerging viral diseases of fish and shrimp. Vet Res 2010; 41:51 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. Barbknecht M, Sepsenwol S, Leis E, Tuttle-Lau M, Gaikowski M et al. Characterization of a new picornavirus isolated from the freshwater fish Lepomis macrochirus. J Gen Virol 2014; 95:601–613 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  26. Lange J, Groth M, Fichtner D, Granzow H, Keller B et al. Virus isolate from carp: genetic characterization reveals a novel picornavirus with two aphthovirus 2A-like sequences. J Gen Virol 2014; 95:80–90 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Phelps NBD, Mor SK, Armien AG, Batts W, Goodwin AE et al. Isolation and molecular characterization of a novel picornavirus from baitfish in the USA. PLoS One 2014; 9:e87593 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  28. Fichtner D, Philipps A, Groth M, Schmidt-Posthaus H, Granzow H et al. Characterization of a novel picornavirus isolate from a diseased European eel (Anguilla anguilla). J Virol 2013; 87:10895–10899 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  29. Hahn MA, Dheilly NM. Genome characterization, prevalence, and transmission mode of a novel picornavirus associated with the threespine stickleback fish (Gasterosteus aculeatus). J Virol 2019; 93:e02277–18 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  30. Altan E, Kubiski SV, Boros Ákos, Reuter G, Sadeghi M et al. A highly divergent picornavirus infecting the gut epithelia of zebrafish (Danio rerio) in research institutions world-wide. Zebrafish 2019; 16:291–299 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  31. Geoghegan JL, Di Giallonardo F, Cousins K, Shi M, Williamson JE et al. Hidden diversity and evolution of viruses in market fish. Virus Evol 2018; 4:vey031 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  32. Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J et al. The evolutionary history of vertebrate RNA viruses. Nature 2018; 556:197–202 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  33. Fautin DG, Allen GR. Field Guide to Anemone Fishes and Their Host Sea Anemones Perth: Western Australian Museum; 1992
    [Google Scholar]
  34. Sin TM, Teo MM, Ng PKL, Chou LM, Khoo HW. The damselfishes (Pisces: Osteichthyes: Pomacentridae) of Peninsular Malaysia and Singapore: systematics, ecology and conservation. Hydrobiologia 1994; 285:49–58 [CrossRef]
    [Google Scholar]
  35. Patkaew S, Direkbusarakom S, Tantithakura O. A simple method for cell culture of ‘Nemo’ ocellaris clownfish (Amphiprion ocellaris, Cuvier 1830). Cell Bio Int Rep 2014; 21:39–45
    [Google Scholar]
  36. King TA. Wild caught ornamental fish: a perspective from the UK ornamental aquatic industry on the sustainability of aquatic organisms and livelihoods. J Fish Biol 2019; 94:925–936 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  37. Watson CA, Shireman JV. Production of Ornamental Aquarium Fish University of Florida IFAS Extension; 2002
    [Google Scholar]
  38. Wabnitz C, Taylor M, Green E, Razak T. From ocean to aquarium: a global trade in marine ornamental species. UNEP world conservation and monitoring centre (WCMC); 2003
  39. Sirajudheen TK, Shyam SS, Bijukumar A, Bindu A. Problems and prospects of marine ornamental fish trade in Kerala, India. J Fish Econ & Dev 2014; 15:14–30
    [Google Scholar]
  40. Yanong R. Personal observation; 2018
  41. Ahasan MS, Subramaniam K, Sayler KA, Loeb JC, Popov VL et al. Molecular characterization of a novel reassortment mammalian orthoreovirus type 2 isolated from a Florida white-tailed deer fawn. Virus Res 2019; 270:197642 [CrossRef]
    [Google Scholar]
  42. Schindelin J, Rueden CT, Hiner MC, Eliceiri KW. The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev 2015; 82:518–529 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  43. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  44. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  45. Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 2014; 9:e108277 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  46. Rivers TM. Viruses and Koch's postulates. J Bacteriol 1937; 33:1–12 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  47. Dee LE, Horii SS, Thornhill DJ. Conservation and management of ornamental coral reef wildlife: successes, shortcomings, and future directions. Biol Conserv 2014; 169:225–237 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001421
Loading
/content/journal/jgv/10.1099/jgv.0.001421
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error