1887

Abstract

is economically a very important species. Recently, promising culture attempts have been made, but a major problem is the uncontrollable mortality during the grow-out phase. As of yet, the life cycle of is not closed in captivity so wild-caught individuals are used for further rearing. Therefore, it is important to investigate the virome of both in wild-caught animals as in cultured animals. In recent years, next-generation-sequencing (NGS) technologies have been very important in the unravelling of the virome of a wide range of environments and matrices, such as soil, sea, potable water, but also of a wide range of animal species. This will be the first report of a virome study in using NGS in combination with the NetoVIR protocol. The near complete genomes of 16 novel viruses were described, most of which were rather distantly related to unclassified viruses or viruses belonging to the , , , , , , , , . A difference in virome composition was observed between muscle and hepatopancreatic tissue, suggesting a distinct tissue tropism of several of these viruses. Some differences in the viral composition were noted between the cultured and wild shrimp, which could indicate that in sub-optimal aquaculture conditions some viruses become more abundant. This research showed that a plethora of unknown viruses is present in and that more research is needed to determine which virus is potentially dangerous for the culture of .

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001412
2020-05-11
2020-06-04
Loading full text...

Full text loading...

/deliver/fulltext/jgv/10.1099/jgv.0.001412/jgv001412.html?itemId=/content/journal/jgv/10.1099/jgv.0.001412&mimeType=html&fmt=ahah

References

  1. Vago C. A virus disease in crustacea. Nat 1966; 209:1290
    [Google Scholar]
  2. Bateman KS, Stentiford GD. A taxonomic review of viruses infecting crustaceans with an emphasis on wild hosts. J Invertebr Pathol 2017; 147:86–110 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  3. Mokili JL, Rohwer F, Dutilh BE. Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2012; 2:63–77 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  4. Gao SJ, Moore PS, Phil M. Molecular approaches to the identification of unculturable infectious agents. Emerg Infect Dis 1996; 2:159–167 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  5. Martínez-Porchas M, Vargas-Albores F. Microbial metagenomics in aquaculture: a potential tool for a deeper insight into the activity. Rev Aquacult 2017; 9:42–56 [CrossRef]
    [Google Scholar]
  6. Handelsman J. Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev 2004; 68:669–685 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  7. Orosco FL, Lluisma AO. Variation in virome diversity in wild populations of Penaeus monodon (Fabricius 1798) with emphasis on pathogenic viruses. Virus Dis 2017; 28:262–271 [CrossRef]
    [Google Scholar]
  8. Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM et al. Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci U S A 2002; 99:14250–14255 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  9. Munang'andu HM. Environmental viral metagenomics analyses in aquaculture: applications in epidemiology and disease control. Front Microbiol 2016; 7:1986 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  10. Williamson SJ. Viral Metagenomics. In Bruijn de. editor Handbook of Molecular Microbial Ecology II: Metagenomics in Different Habitats Wiley-Blackwell; 2011 pp 4–12
    [Google Scholar]
  11. Alavandi SV, Poornima M. Viral metagenomics: a tool for virus discovery and diversity in aquaculture. Indian J Virol 2012; 23:88–98 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  12. Liu S, Chen Y, Bonning BC. RNA virus discovery in insects. Insect Sci 2015; 8:54–61 [CrossRef]
    [Google Scholar]
  13. Shi C, Beller L, Deboutte W, Yinda KC, Delang L et al. Stable distinct core eukaryotic viromes in different mosquito species from Guadeloupe, using single mosquito viral metagenomics. Microbiome 2019; 7:121 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  14. Sritunyalucksana K, Apisawetakan S, Boon-Nat A, Withyachumnarnkul B, Flegel TW. A new RNA virus found in black tiger shrimp Penaeus monodon from Thailand. Virus Res 2006; 118:31–38 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  15. Ng TF, Alavandi S, Varsani A, Burghart S, Breitbart M. Metagenomic identification of a nodavirus and a circular ssDNA virus in semi-purified viral nucleic acids from the hepatopancreas of healthy Farfantepenaeus duorarum shrimp. Dis Aquat Organ 2013; 105:237–242 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  16. Dunlap DS, Ng TFF, Rosario K, Barbosa JG, Greco AM et al. Molecular and microscopic evidence of viruses in marine copepods. Proc Natl Acad Sci U S A 2013; 110:1375–1380 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  17. Rosani U, Gerdol M. A bioinformatics approach reveals seven nearly-complete RNA-virus genomes in bivalve RNA-Seq data. Virus Res 2017; 239:33–42 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  18. Gudenkauf BM, Hewson I. Comparative metagenomics of viral assemblages inhabiting four phyla of marine invertebrates. Front Mar Sci 2016; 3: [CrossRef]
    [Google Scholar]
  19. Hewson I, Brown JM, Burge CA, Couch CS, LaBarre BA et al. Description of viral assemblages associated with the Gorgonia ventalina holobiont. Coral Reefs 2012; 31:487–491 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  20. Hewson I, Eaglesham JB, Höök TO, LaBarre BA, Sepúlveda MS et al. Investigation of viruses in Diporeia spp. from the Laurentian great lakes and Owasco lake as potential stressors of declining populations. J Great Lakes Res 2013; 39:499–506 [CrossRef]
    [Google Scholar]
  21. Gudenkauf BM, Eaglesham JB, Aragundi WM, Hewson I. Discovery of urchin-associated densoviruses (family Parvoviridae) in coastal waters of the Big Island, Hawaii. J Gen Virol 2014; 95:652–658 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  22. Hewson I, Button JB, Gudenkauf BM, Miner B, Newton AL et al. Densovirus associated with sea-star wasting disease and mass mortality. Proc Natl Acad Sci U S A 2014; 111:17278–17283 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  23. Li C-X, Shi M, Tian J-H, Lin X-D, Kang Y-J et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife 2015; 4:e05378 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  24. Rosario K, Schenck RO, Harbeitner RC, Lawler SN, Breitbart M. Novel circular single-stranded DNA viruses identified in marine invertebrates reveal high sequence diversity and consistent predicted intrinsic disorder patterns within putative structural proteins. Front Microbiol 2015; 6:696 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  25. Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X et al. Redefining the invertebrate RNA virosphere. Nature 2016; 540:539–543 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  26. Walker PJ, Winton JR. Emerging viral diseases of fish and shrimp. Vet Res 2010; 41:51 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  27. Walker PJ, Mohan CV. Viral disease emergence in shrimp aquaculture: origins, impact and the effectiveness of health management strategies. Rev Aquacult 2009; 1:125–154 [CrossRef]
    [Google Scholar]
  28. Van Eynde B, Vuylsteke D, Christiaens O, Cooreman K, Smagghe G et al. Improvements in larviculture of Crangon crangon as a step towards its commercial aquaculture. Aquac Res 2019; 50:1658–1667 [CrossRef]
    [Google Scholar]
  29. Stentiford GD, Feist SW. A histopathological survey of shore crab (Carcinus maenas) and brown shrimp (Crangon crangon) from six estuaries in the United Kingdom. J Invertebr Pathol 2005; 88:136–146 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  30. Van Eynde B, Christiaens O, Delbare D, Cooreman K, Bateman KS et al. Development and application of a duplex PCR assay for detection of Crangon crangon bacilliform virus in populations of European brown shrimp (Crangon crangon). J Invertebr Pathol 2018; 153:195–202 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  31. Soetaert M, Chiers K, Duchateau L, Polet H, Verschueren B et al. Determining the safety range of electrical pulses for two benthic invertebrates: Brown shrimp (Crangon crangon L.) and ragworm (Alitta virens S.). ICES J Mar Sci 2015; 72:973–980 [CrossRef]
    [Google Scholar]
  32. Conceição-Neto N, Zeller M, Lefrère H, De Bruyn P, Beller L et al. Modular approach to customise sample preparation procedures for viral metagenomics: a reproducible protocol for virome analysis. Sci Rep 2015; 5:16532 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  33. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using diamond. Nat Methods 2015; 12:59–60 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  34. Yinda CK, Zeller M, Conceição-Neto N, Maes P, Deboutte W et al. Novel highly divergent reassortant bat rotaviruses in Cameroon, without evidence of zoonosis. Sci Rep 2016; 6:34209 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  35. Yinda CK, Rector A, Zeller M, Conceição-Neto N, Heylen E et al. A single bat species in Cameroon harbors multiple highly divergent papillomaviruses in stool identified by metagenomics analysis. Virol Rep 2016; 6:74–80 [CrossRef]
    [Google Scholar]
  36. Yinda CK, Conceição-Neto N, Zeller M, Heylen E, Maes P et al. Novel highly divergent sapoviruses detected by metagenomics analysis in straw-colored fruit bats in Cameroon. Emerg Microbes Infect 2017; 6:e381–7 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  37. Yinda CK, Zell R, Deboutte W, Zeller M, Conceição-Neto N et al. Highly diverse population of Picornaviridae and other members of the Picornavirales, in Cameroonian fruit bats. BMC Genomics 2017; 18:249 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  38. Ondov BD, Bergman NH, Phillippy AM. Interactive metagenomic visualization in a web browser. BMC Bioinformatics 2011; 12:385 [CrossRef]
    [Google Scholar]
  39. Maric J. Long read RNA-Seq mapper (Master thesis) Zagreb, Croatia: University of Zagreb; 2017 p 62
    [Google Scholar]
  40. Paulson JN. MetagenomeSeq: Statistical Analysis for Sparse High-Throughput Sequencing (Vignette) United States: University of Maryland; 2019 p 35
    [Google Scholar]
  41. Guu TSY, Zheng W, Tao YJ. Bunyavirus: structure and replication. Adv Exp Med Biol 2012; 726:245–266 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  42. Elliott RM. Molecular biology of the Bunyaviridae. J Gen Virol 1990; 71 (Pt 3:501–522 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  43. Schmaljohn CS, Nichol ST. Bunyaviridae. In Knipe DM, Howley PM. (editors) Field’s Virology Philadelphia, PA: Lippincott Wiliams & Wilkins Co; 2007 pp 1741–1789
    [Google Scholar]
  44. Elliot RM, Schmaljohn C. Bunyaviridae. In Knipe DM, Howley PM. (editors) Field’s Virology Philadelphia, PA: Lippincott Wiliams & Wilkins Co; 2013 pp 1244–1282
    [Google Scholar]
  45. Elliott RM. Orthobunyaviruses: recent genetic and structural insights. Nat Rev Microbiol 2014; 12:673–685 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  46. Shi M, Lin X-D, Vasilakis N, Tian J-H, Li C-X, Chen LJ et al. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J Virol 2016; 90:659–669 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  47. Parry R, Asgari S. Discovery of novel crustacean and cephalopod flaviviruses: insights into the evolution and circulation of flaviviruses between marine invertebrate and vertebrate hosts. J Virol 2019; 93:e00432–19 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  48. Le Gall O, Christian P, Fauquet CM, King AMQ, Knowles NJ et al. Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T = 3 virion architecture. Arch Virol 2008; 153:715–727 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  49. Scheets K, Jordan R, White KA, Hernández C. Pelarspovirus, a proposed new genus in the family Tombusviridae. Arch Virol 2015; 160:2385–2393 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  50. Bonami J-R, Zhang S. Viral diseases in commercially exploited crabs: a review. J Invertebr Pathol 2011; 106:6–17 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  51. Olivier V, Blanchard P, Chaouch S, Lallemand P, Schurr F et al. Molecular characterisation and phylogenetic analysis of chronic bee paralysis virus, a honey bee virus. Virus Res 2008; 132:59–68 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  52. Sõmera M, Sarmiento C, Truve E. Overview on Sobemoviruses and a proposal for the creation of the family Sobemoviridae. Viruses 2015; 7:3076–3115 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  53. Hillman BI, Cai G. The family narnaviridae: simplest of RNA viruses. Adv Virus Res 2013; 86:149–176 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  54. Stentiford GD, Bateman K, Feist SW. Pathology and ultrastructure of an intranuclear bacilliform virus (IBV) infecting brown shrimp Crangon crangon (Decapoda: Crangonidae). Dis Aquat Organ 2004; 58:89–97 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  55. Fauver JR, Grubaugh ND, Krajacich BJ, Weger-Lucarelli J, Lakin SM et al. West African Anopheles gambiae mosquitoes harbor a taxonomically diverse virome including new insect-specific flaviviruses, mononegaviruses and totiviruses. Virology 2016; 498:288–299 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  56. Laureti M, Narayanan D, Rodriguez-Andres J, Fazakerley JK, Kedzierski L. Flavivirus receptors: diversity, identity, and cell entry. Front Immunol 2018; 9:2180 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  57. Sakuna K, Elliman J, Tzamouzaki A, Owens L. A novel virus (order Bunyavirales) from stressed redclaw crayfish (Cherax quadricarinatus) from farms in northern Australia. Virus Res 2018; 250:7–12 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  58. Bonami J-R, Shi Z, Qian D, Sri Widada J, Widada JS. White tail disease of the giant freshwater prawn, Macrobrachium rosenbergii: separation of the associated virions and characterization of MrNV as a new type of nodavirus. J Fish Dis 2005; 28:23–31 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  59. Tang KFJ, Pantoja CR, Redman RM, Navarro SA, Lightner DV. Ultrastructural and sequence characterization of Penaeus vannamei nodavirus (PvNV) from Belize. Dis Aquat Organ 2011; 94:179–187 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  60. Cornejo-Granados F, Lopez-Zavala AA, Gallardo-Becerra L, Mendoza-Vargas A, Sánchez F et al. Microbiome of Pacific whiteleg shrimp reveals differential bacterial community composition between wild, aquacultured and AHPND/EMS outbreak conditions. Sci Rep 2017; 7:11783 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  61. Chen Y-H, He J-G. Effects of environmental stress on shrimp innate immunity and white spot syndrome virus infection. Fish Shellfish Immunol 2019; 84:744–755 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  62. Lightner DV. Virus diseases of farmed shrimp in the Western hemisphere (the Americas): a review. J Invertebr Pathol 2011; 106:110–130 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  63. Bojko J, Subramaniam K, Waltzek TB, Stentiford GD, Behringer DC. Genomic and developmental characterisation of a novel bunyavirus infecting the crustacean Carcinus maenas. Sci Rep 2019; 9:12957 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  64. Grandjean F, Gilbert C, Razafimafondy F, Vucić M, Delaunay C et al. A new bunya-like virus associated with mass mortality of white-clawed crayfish in the wild. Virology 2019; 533:115–124 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  65. Khawsak P, Deesukon W, Chaivisuthangkura P, Sukhumsirichart W. Multiplex RT-PCR assay for simultaneous detection of six viruses of penaeid shrimp. Mol Cell Probes 2008; 22:177–183 [CrossRef][PubMed][PubMed]
    [Google Scholar]
  66. Meeus I, Smagghe G, Siede R, Jans K, de Graaf DC. Multiplex RT-PCR with broad-range primers and an exogenous internal amplification control for the detection of honeybee viruses in bumblebees. J Invertebr Pathol 2010; 105:200–203 [CrossRef][PubMed][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001412
Loading
/content/journal/jgv/10.1099/jgv.0.001412
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