1887

Abstract

Echinoderms are a phylum of marine invertebrates that include model organisms, keystone species, and animals commercially harvested for seafood. Despite their scientific, ecological, and economic importance, there is little known about the diversity of RNA viruses that infect echinoderms compared to other invertebrates. We screened over 900 transcriptomes and viral metagenomes to characterize the RNA virome of 38 echinoderm species from all five classes (Crinoidea, Holothuroidea, Asteroidea, Ophiuroidea and Echinoidea). We identified 347 viral genome fragments that were classified to genera and families within nine viral orders - and . We compared the relative viral representation across three life stages (embryo, larvae, adult) and characterized the gene content of contigs which encoded complete or near-complete genomes. The proportion of viral reads in a given transcriptome was not found to significantly differ between life stages though the majority of viral contigs were discovered from transcriptomes of adult tissue. This study illuminates the biodiversity of RNA viruses from echinoderms, revealing the occurrence of viral groups in natural populations.

Funding
This study was supported by the:
  • Andrew W. Mellon Foundation
    • Principle Award Recipient: ElliotWalter Jackson
  • Cornell Atkinson Center for Sustainability, Cornell University
    • Principle Award Recipient: ElliotWalter Jackson
  • Directorate for Geosciences (Award OCE-2049225)
    • Principle Award Recipient: IanHewson
  • Division of Ocean Sciences (Award OCE-1737127)
    • Principle Award Recipient: IanHewson
  • Division of Ocean Sciences (Award OCE-1537111)
    • Principle Award Recipient: IanHewson
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001772
2022-06-29
2024-04-23
Loading full text...

Full text loading...

References

  1. 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 [View Article] [PubMed]
    [Google Scholar]
  2. 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 [View Article] [PubMed]
    [Google Scholar]
  3. Bekal S, Domier LL, Gonfa B, McCoppin NK, Lambert KN et al. A novel flavivirus in the soybean cyst nematode. J Gen Virol 2014; 95:1272–1280 [View Article] [PubMed]
    [Google Scholar]
  4. 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 [View Article] [PubMed]
    [Google Scholar]
  5. Qin X-C, Shi M, Tian J-H, Lin X-D, Gao D-Y et al. A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors. Proc Natl Acad Sci U S A 2014; 111:6744–6749 [View Article] [PubMed]
    [Google Scholar]
  6. Shi M, Lin X-D, Vasilakis N, Tian J-H, Li C-X 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 [View Article] [PubMed]
    [Google Scholar]
  7. Junglen S, Drosten C. Virus discovery and recent insights into virus diversity in arthropods. Curr Opin Microbiol 2013; 16:507–513 [View Article] [PubMed]
    [Google Scholar]
  8. 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: [View Article] [PubMed]
    [Google Scholar]
  9. Liu S, Chen Y, Bonning BC. RNA virus discovery in insects. Curr Opin Insect Sci 2015; 8:54–61 [View Article] [PubMed]
    [Google Scholar]
  10. Remnant EJ, Shi M, Buchmann G, Blacquière T, Holmes EC et al. A Diverse Range of Novel RNA Viruses in Geographically Distinct Honey Bee Populations. J Virol 2017; 91:e00158-17 [View Article] [PubMed]
    [Google Scholar]
  11. Käfer S, Paraskevopoulou S, Zirkel F, Wieseke N, Donath A et al. Re-assessing the diversity of negative strand RNA viruses in insects. PLoS Pathog 2019; 15:e1008224 [View Article] [PubMed]
    [Google Scholar]
  12. Wu H, Pang R, Cheng T, Xue L, Zeng H et al. Abundant and Diverse RNA Viruses in Insects Revealed by RNA-Seq Analysis: Ecological and Evolutionary Implications. mSystems 2020; 5:e00039-20 [View Article] [PubMed]
    [Google Scholar]
  13. Wang YN, Chang YQ, Lawrence JM. Chapter 12 - Disease in Sea Urchins. In Lawrence JM. eds Developments in Aquaculture and Fisheries Science Elsevier; pp 179–186
    [Google Scholar]
  14. Hewson I, Sullivan B, Jackson EW, Xu Q, Long H et al. Perspective: something old, something new? Review of wasting and other mortality in Asteroidea (Echinodermata). Front Mar Sci 2019; 6:406 [View Article]
    [Google Scholar]
  15. Slater M. Use and Exploitation of Sea Cucumbers. In Echinoderm Aquaculture John Wiley & Sons, Ltd; pp 57–73
    [Google Scholar]
  16. Brown NP, Eddy SD. Use and Exploitation of Sea Urchins Hoboken, NJ, USA: Echinoderm Aquaculture. John Wiley & Sons, Ltd; pp 25–45
    [Google Scholar]
  17. Deng H, Zhou Z, Wang N, Liu C. The syndrome of sea cucumber (Apostichopus japonicus) infected by virus and bacteria. Virol Sin 2008; 23:63–67 [View Article]
    [Google Scholar]
  18. Liu H, Zheng F, Sun X, Hong X, Dong S et al. Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). J Invertebr Pathol 2010; 105:236–242 [View Article] [PubMed]
    [Google Scholar]
  19. 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 [View Article] [PubMed]
    [Google Scholar]
  20. Jackson EW, Bistolas KSI, Button JB, Hewson I. Novel circular single-stranded DNA viruses among an asteroid, echinoid and holothurian (Phylum: Echinodermata). PLoS One 2016; 11:e0166093 [View Article] [PubMed]
    [Google Scholar]
  21. Hewson I, Aquino CA, DeRito CM. Virome variation during sea star wasting disease progression in Pisaster ochraceus (Asteroidea, Echinodermata). Viruses 2020; 12:E1332 [View Article] [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 [View Article] [PubMed]
    [Google Scholar]
  23. Bucci C, Francoeur M, McGreal J, Smolowitz R, Zazueta-Novoa V et al. Sea star wasting disease in Asterias forbesi along the Atlantic Coast of North America. PLoS One 2017; 12:e0188523 [View Article] [PubMed]
    [Google Scholar]
  24. Hewson I, Bistolas KSI, Quijano Cardé EM, Button JB, Foster PJ et al. Investigating the complex association between viral ecology, environment, and Northeast Pacific Sea Star Wasting. Front Mar Sci 2018; 5:77 [View Article]
    [Google Scholar]
  25. Jackson EW, Pepe-Ranney C, Johnson MR, Distel DL, Hewson I. A highly prevalent and pervasive densovirus discovered among sea stars from the North American Atlantic Coast. Appl Environ Microbiol 2020; 86:e02723-19 [View Article] [PubMed]
    [Google Scholar]
  26. Jackson EW, Wilhelm RC, Johnson MR, Lutz HL, Danforth I et al. Diversity of sea star-associated densoviruses and transcribed endogenous viral Elements of densovirus origin. J Virol 2020; 95:e01594-20 [View Article] [PubMed]
    [Google Scholar]
  27. Hewson I, Johnson MR, Tibbetts IR. An unconventional Flavivirus and other RNA viruses in the sea cucumber (Holothuroidea; Echinodermata) Virome. Viruses 2020; 12:E1057 [View Article] [PubMed]
    [Google Scholar]
  28. Shi M, Zhang Y-Z, Holmes EC. Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res 2018; 243:83–90 [View Article] [PubMed]
    [Google Scholar]
  29. Waldron FM, Stone GN, Obbard DJ. Metagenomic sequencing suggests a diversity of RNA interference-like responses to viruses across multicellular eukaryotes. PLoS Genet 2018; 14:e1007533 [View Article] [PubMed]
    [Google Scholar]
  30. Wu H, Pang R, Cheng T, Xue L, Zeng H et al. Abundant and diverse RNA viruses in insects revealed by RNA-Seq analysis: ecological and evolutionary implications. mSystems 2020; 5:e00039-20 [View Article] [PubMed]
    [Google Scholar]
  31. Parry R, Asgari S, Williams BRG. 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 [View Article] [PubMed]
    [Google Scholar]
  32. Cheng R-L, Li X-F, Zhang C-X. Novel dicistroviruses in an unexpected wide range of invertebrates. Food Environ Virol 2021; 13:423–431 [View Article] [PubMed]
    [Google Scholar]
  33. Zhang Y-Z, Chen Y-M, Wang W, Qin X-C, Holmes EC. Expanding the RNA virosphere by unbiased metagenomics. Annu Rev Virol 2019; 6:119–139 [View Article] [PubMed]
    [Google Scholar]
  34. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  35. Gordon A, Fastx-toolkit HGJ. FASTQ/A short-reads preprocessing tools; 2010 http://hannonlab.cshl.edu/fastx_toolkit
  36. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011; 29:644–652 [View Article] [PubMed]
    [Google Scholar]
  37. Bushnell B. BBTools software package. http://sourceforge net/projects/bbmap 2014;578:579
  38. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  39. Wolf YI, Silas S, Wang Y, Wu S, Bocek M et al. Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome. Nat Microbiol 2020; 5:1262–1270 [View Article] [PubMed]
    [Google Scholar]
  40. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods 2015; 12:59–60 [View Article] [PubMed]
    [Google Scholar]
  41. Bushnell B. BBMap: A Fast, Accurate Splice-Aware Aligner;
    [Google Scholar]
  42. Gerlt JA, Bouvier JT, Davidson DB, Imker HJ, Sadkhin B et al. Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): A web tool for generating protein sequence similarity networks. Biochim Biophys Acta 2015; 1854:1019–1037 [View Article] [PubMed]
    [Google Scholar]
  43. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [View Article] [PubMed]
    [Google Scholar]
  44. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  45. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
    [Google Scholar]
  46. Rambaut A, Drummond A. FigTree: Tree Figure Drawing Tool, Version 1.2. 2 Institute of Evolutionary Biology, University of Edinburgh;
    [Google Scholar]
  47. Paraskevopoulou S, Käfer S, Zirkel F, Donath A, Petersen M et al. Viromics of extant insect orders unveil the evolution of the flavi-like superfamily. Virus Evol 2021; 7:veab030 [View Article] [PubMed]
    [Google Scholar]
  48. Bergner LM, Orton RJ, Benavides JA, Becker DJ, Tello C et al. Demographic and environmental drivers of metagenomic viral diversity in vampire bats. Mol Ecol 2020; 29:26–39 [View Article] [PubMed]
    [Google Scholar]
  49. Wille M, Shi M, Hurt AC, Klaassen M, Holmes EC. RNA virome abundance and diversity is associated with host age in a bird species. Virology 2021; 561:98–106 [View Article] [PubMed]
    [Google Scholar]
  50. Culley AI, Lang AS, Suttle CA. High diversity of unknown picorna-like viruses in the sea. Nature 2003; 424:1054–1057 [View Article] [PubMed]
    [Google Scholar]
  51. Zhang Y-Y, Chen Y, Wei X, Cui J. Viromes in marine ecosystems reveal remarkable invertebrate RNA virus diversity. Sci China Life Sci 2022; 65:426–437 [View Article]
    [Google Scholar]
  52. Lang AS, Vlok M, Culley AI, Suttle CA, Takao Y et al. ICTV virus taxonomy profile: Marnaviridae 2021. J Gen Virol 2021; 102:001633 [View Article] [PubMed]
    [Google Scholar]
  53. Brussaard CPD, Noordeloos AAM, Sandaa R-A, Heldal M, Bratbak G. Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla. Virology 2004; 319:280–291 [View Article] [PubMed]
    [Google Scholar]
  54. Day JM. The diversity of the orthoreoviruses: molecular taxonomy and phylogentic divides. Infect Genet Evol 2009; 9:390–400 [View Article] [PubMed]
    [Google Scholar]
  55. Valles SM, Chen Y, Firth AE, Guérin DMA, Hashimoto Y et al. ICTV virus taxonomy profile: Iflaviridae. J Gen Virol 2017; 98:527–528 [View Article] [PubMed]
    [Google Scholar]
  56. Guo L, Lu X, Liu X, Li P, Wu J et al. Meta-transcriptomic analysis reveals the virome and viral genomic evolution of medically important mites. J Virol 2020JVI.01686-20 [View Article] [PubMed]
    [Google Scholar]
  57. Steil BP, Kempf BJ, Barton DJ. Poly(A) at the 3’ end of positive-strand RNA and VPg-linked poly(U) at the 5’ end of negative-strand RNA are reciprocal templates during replication of poliovirus RNA. J Virol 2010; 84:2843–2858 [View Article] [PubMed]
    [Google Scholar]
  58. Visser M, Bester R, Burger JT, Maree HJ. Next-generation sequencing for virus detection: covering all the bases. Virol J 2016; 13:1–6 [View Article] [PubMed]
    [Google Scholar]
  59. Gann ER, Kang Y, Dyhrman ST, Gobler CJ, Wilhelm SW. Metatranscriptome library preparation influences analyses of viral community activity during a brown tide bloom. Front Microbiol 2021; 12:664189 [View Article] [PubMed]
    [Google Scholar]
  60. Canuti M, van der Hoek L. Virus discovery: are we scientists or genome collectors?. Trends Microbiol 2014; 22:229–231 [View Article] [PubMed]
    [Google Scholar]
  61. Greninger AL. A decade of RNA virus metagenomics is (not) enough. Virus Res 2018; 244:218–229 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001772
Loading
/content/journal/jgv/10.1099/jgv.0.001772
Loading

Data & Media loading...

Supplements

Supplementary material 1

EXCEL

Supplementary material 2

EXCEL

Supplementary material 3

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