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
Open Access articles citing this article.
Nature Communications Open Access 28 June 2017
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Pallansch, M. A. & Roos, R. P. in Fields Virology (eds Knipe, D. M. & Howley, P. M.) 723–775 (Lippincott, Williams & Wilkins, Philadelphia, 2001)
Lazarowitz, S. G. in Fields Virology (eds Knipe, D. M. & Howley, P. M.) 533–598 (Lippincott, Williams & Wilkins, Philadelphia, PA, 2001)
Bailey, L., Gibbs, A. J. & Woods, R. D. Sacbrood virus of the larval honey bee (Apis mellifera Linnaeus). Virology 23, 425–429 (1964)
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)
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)
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)
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)
Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548 (1999)
Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea. Bioscience 49, 781–788 (1999)
Suttle, C. A. in Viral Ecology (ed. Hurst, C. J.) 248–286 (Academic, San Diego, CA, 2000)
Wommack, K. E. & Colwell, R. R. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114 (2000)
Mann, N. H. Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol. Rev. 27, 17–34 (2003)
Bernard, J. & Bremont, M. Molecular biology of fish viruses — a review. Vet. Res. 26, 341–351 (1995)
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)
Smith, A. in Viral Ecology (ed. Hurst, C.) 447–491 (Academic, San Diego, CA, 2000)
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)
Koonin, E. V. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72, 2197–2206 (1991)
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)
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)
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)
Kamer, G. & Argos, P. Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res. 12, 7269–7282 (1984)
Tai, V. et al. Characterization of HaRNAV, a single-stranded RNA virus causing lysis of Heterosigma akashiwo (Raphidophyceae). J. Phycol. 39, 343–352 (2003)
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)
Suttle, C. A. & Chen, F. Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58, 3721–3729 (1992)
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)
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)
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)
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)
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)
Fitch, W. M. & Margoliash, E. Construction of phylogenetic trees. Science 155, 279–284 (1967)
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.
The authors declare that they have no competing financial interests.
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
Complete genome analysis of a novel picorna-like virus from a ladybird beetle (Cheilomenes sexmaculata)
Archives of Virology (2022)
Nature Communications (2017)
Nature Reviews Microbiology (2017)
Nature Reviews Microbiology (2015)
Shotgun metagenomics indicates novel family A DNA polymerases predominate within marine virioplankton
The ISME Journal (2014)