Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

High diversity of unknown picorna-like viruses in the sea

Abstract

Picorna-like viruses are a loosely defined group of positive-sense single-stranded RNA viruses that are major pathogens of animals, plants and insects. They include viruses that are of enormous economic and public-health concern and are responsible for animal diseases (such as poliomyelitis1), plant diseases (such as sharka2) and insect diseases (such as sacbrood3). Viruses from the six divergent families (the Picornaviridae, Caliciviridae, Comoviridae, Sequiviridae, Dicistroviridae and Potyviridae) that comprise the picorna-like virus superfamily4 have the following features in common: a genome with a protein attached to the 5′ end and no overlapping open reading frames, all the RNAs are translated into a polyprotein before processing, and a conserved RNA-dependent RNA polymerase (RdRp) protein. Analyses of RdRp sequences from these viruses produce phylogenies that are congruent with established picorna-like virus family assignments5,6,7; hence, this gene is an excellent molecular marker for examining the diversity of picorna-like viruses in nature. Here we report, on the basis of analysis of RdRp sequences amplified from marine virus communities, that a diverse array of picorna-like viruses exists in the ocean. All of the sequences amplified were divergent from known picorna-like viruses, and fell within four monophyletic groups that probably belong to at least two new families. Moreover, we show that an isolate belonging to one of these groups is a lytic pathogen of Heterosigma akashiwo, a toxic-bloom-forming alga responsible for severe economic losses to the finfish aquaculture industry, suggesting that picorna-like viruses are important pathogens of marine phytoplankton.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Maximum-likelihood tree of RdRp sequences from environmental amplicons and representative viruses from picorna-like virus families.

Similar content being viewed by others

References

  1. Pallansch, M. A. & Roos, R. P. in Fields Virology (eds Knipe, D. M. & Howley, P. M.) 723–775 (Lippincott, Williams & Wilkins, Philadelphia, 2001)

    Google Scholar 

  2. Lazarowitz, S. G. in Fields Virology (eds Knipe, D. M. & Howley, P. M.) 533–598 (Lippincott, Williams & Wilkins, Philadelphia, PA, 2001)

    Google Scholar 

  3. Bailey, L., Gibbs, A. J. & Woods, R. D. Sacbrood virus of the larval honey bee (Apis mellifera Linnaeus). Virology 23, 425–429 (1964)

    Article  CAS  Google Scholar 

  4. Liljas, L. et al. Evolutionary and taxonomic implications of conserved structural motifs between picornaviruses and insect picorna-like viruses. Arch. Virol. 147, 59–84 (2002)

    Article  CAS  Google Scholar 

  5. Koonin, E. V. & Dolja, V. V. Evolution and taxonomy of positive-strand RNA viruses - implications of comparative-analysis of amino-acid-sequences. Crit. Rev. Biochem. Mol. Biol. 28, 375–430 (1993)

    Article  CAS  Google Scholar 

  6. Zanotto, P. M. D., Gibbs, M. J., Gould, E. A. & Holmes, E. C. A reevaluation of the higher taxonomy of viruses based on RNA polymerases. J. Virol. 70, 6083–6096 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Mari, J., Poulos, B. T., Lightner, D. V. & Bonami, J. R. Shrimp Taura syndrome virus: genomic characterization and similarity with members of the genus Cricket paralysis-like viruses. J. Gen. Virol. 83, 915–926 (2002)

    Article  CAS  Google Scholar 

  8. Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548 (1999)

    Article  ADS  CAS  Google Scholar 

  9. Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea. Bioscience 49, 781–788 (1999)

    Article  Google Scholar 

  10. Suttle, C. A. in Viral Ecology (ed. Hurst, C. J.) 248–286 (Academic, San Diego, CA, 2000)

    Google Scholar 

  11. Wommack, K. E. & Colwell, R. R. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114 (2000)

    Article  CAS  Google Scholar 

  12. Mann, N. H. Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol. Rev. 27, 17–34 (2003)

    Article  CAS  Google Scholar 

  13. Bernard, J. & Bremont, M. Molecular biology of fish viruses — a review. Vet. Res. 26, 341–351 (1995)

    CAS  PubMed  Google Scholar 

  14. Van Bressem, M. F., Van Waerebeek, K. & Raga, J. A. A review of virus infections of cetaceans and the potential impact of morbilliviruses, poxviruses and papillomaviruses on host population dynamics. Dis. Aquat. Organ. 38, 53–65 (1999)

    Article  CAS  Google Scholar 

  15. Smith, A. in Viral Ecology (ed. Hurst, C.) 447–491 (Academic, San Diego, CA, 2000)

    Book  Google Scholar 

  16. Poch, O., Sauvaget, I., Delarue, M. & Tordo, N. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J. 8, 3867–3874 (1989)

    Article  CAS  Google Scholar 

  17. Koonin, E. V. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72, 2197–2206 (1991)

    Article  Google Scholar 

  18. Suttle, C. A., Chan, A. M. & Cottrell, M. T. Use of ultrafiltration to isolate viruses from seawater which are pathogens of marine phytoplankton. Appl. Environ. Microbiol. 57, 721–726 (1991)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997)

    Article  CAS  Google Scholar 

  20. Kingsley, D. H., Meade, G. K. & Richards, G. P. Detection of both hepatitis a virus and Norwalk-like virus in imported clams associated with food-borne illness. Appl. Environ. Microbiol. 68, 3914–3918 (2002)

    Article  CAS  Google Scholar 

  21. Kamer, G. & Argos, P. Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res. 12, 7269–7282 (1984)

    Article  CAS  Google Scholar 

  22. Tai, V. et al. Characterization of HaRNAV, a single-stranded RNA virus causing lysis of Heterosigma akashiwo (Raphidophyceae). J. Phycol. 39, 343–352 (2003)

    Article  CAS  Google Scholar 

  23. Smayda, T. J. in Physiological Ecology of Harmful Algal Blooms (eds Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M.) 113–131 (Springer, Berlin, GER, 1998)

    Google Scholar 

  24. Suttle, C. A. & Chen, F. Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58, 3721–3729 (1992)

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Smith, A. W., Akers, T. G., Madiu, S. H. & Vedros, N. A. San Miguel sea lion virus isolation, preliminary characterization and relationship to vesicular exanthema of swine virus. Nature 244, 108–110 (1973)

    Article  ADS  CAS  Google Scholar 

  26. Short, S. M. & Suttle, C. A. Sequence analysis of marine virus communities reveals that groups of related algal viruses are widely distributed in nature. Appl. Environ. Microbiol. 68, 1290–1296 (2002)

    Article  CAS  Google Scholar 

  27. Thompson, J. D. et al. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24, 4876–4882 (1997)

    Article  ADS  Google Scholar 

  28. Whelan, S. & Goldman, N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691–699 (2001)

    Article  CAS  Google Scholar 

  29. Schmidt, H. A., Strimmer, K., Vingron, M. & von Haeseler, A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504 (2002)

    Article  CAS  Google Scholar 

  30. Fitch, W. M. & Margoliash, E. Construction of phylogenetic trees. Science 155, 279–284 (1967)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank the crew and participants of the SOG cruises from 1996 to 1998. We also thank C. Frederickson for assistance with DGGE and M. Berbee and P. Keeling for advice on phylogenetic analyses. This work was supported by a National Science and Engineering Research Council of Canada grant to C.A.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Curtis A. Suttle.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Culley, A., Lang, A. & Suttle, C. High diversity of unknown picorna-like viruses in the sea. Nature 424, 1054–1057 (2003). https://doi.org/10.1038/nature01886

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01886

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing