Metagenomic analysis of the shrew enteric virome reveals novel viruses related to human stool-associated viruses

Journal of General Virology

Volumn 96, Issue 2, 2015, Pages 440-452

  Sasaki, Michihito ^a   Orba, Yasuko ^a   Ueno, Keisuke ^a   Ishii, Akihiro ^b   Moonga, Ladslav ^c   Hangombe, Bernard M ^c   Mweene, Aaron S ^c   Ito, Kimihito ^a   Sawa, Hirofumi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b Hokudai Center for Zoonosis Control in Zambia   (Zambia)

^c UNIVERSITY OF ZAMBIA   (Zambia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CALHEVIRUS; CEREBROSPINAL FLUID; CONTROLLED STUDY; CROCIDURA; CYCLOVIRUS; ENTERIC VIROME; FECES; GENE SEQUENCE; GENOME ANALYSIS; HIGH THROUGHPUT SEQUENCING; INSECT VIRUS; METAGENOMICS; MICROBIOLOGICAL PARAMETERS; NEW GENUS; NONHUMAN; PARECHOVIRUS; PICORNA LIKE VIRUS; PICORNAVIRIDAE; PRIORITY JOURNAL; SHREW; ANIMAL; BIOTA; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; INTESTINE; METAGENOME; MOLECULAR GENETICS; PHYLOGENY; VIROLOGY; VIRUS;

CROCIDURA; HEXAPODA; HUMAN PARECHOVIRUS; MAMMALIA; PICORNAVIRIDAE; RODENTIA; SORICIDAE;

ANIMALS; BIOTA; CLUSTER ANALYSIS; INTESTINES; METAGENOME; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SHREWS; VIRUSES;

EID: 84921766948     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.071209-0     Document Type: Article

References (86)

1. Adams, M. J., King, A. M. Q. & Carstens, E. B. (2013). Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2013). Arch Virol 158, 2023-2030.
2. Allander, T., Emerson, S. U., Engle, R. E., Purcell, R. H. & Bukh, J. (2001). A virus discovery method incorporating DNase treatment and its application to the identification of two bovine parvovirus species. Proc Natl Acad Sci U S A 98, 11609-11614.
3. Anthony, S. J., Epstein, J. H., Murray, K. A., Navarrete-Macias, I., Zambrana-Torrelio, C. M., Solovyov, A., Ojeda-Flores, R., Arrigo, N. C., Islam, A. & other authors (2013). A strategy to estimate unknown viral diversity in mammals. MBio 4, e00598-e13.
4. Baker, K. S., Leggett, R. M., Bexfield, N. H., Alston, M., Daly, G., Todd, S., Tachedjian, M., Holmes, C. E., Crameri, S. & other authors (2013). Metagenomic study of the viruses of African straw-coloured fruit bats: detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology 441, 95-106.
5. Blom, N., Hansen, J., Brunak, S. & Blaas, D. (1996). Cleavage site analysis in picornaviral polyproteins: discovering cellular targets by neural networks. Protein Sci 5, 2203-2216.
6. Bodewes, R., van der Giessen, J., Haagmans, B. L., Osterhaus, A. D. & Smits, S. L. (2013). Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes. J Virol 87, 7758-7764.
7. Bonning, B. C. & Miller, W. A. (2010). Dicistroviruses. Annu Rev Entomol 55, 129-150.
8. Boros, Á., Nemes, C., Pankovics, P., Kapusinszky, B., Delwart, E. & Reuter, G. (2012). Identification and complete genome characterization of a novel picornavirus in turkey (Meleagris gallopavo). J Gen Virol 93, 2171-2182.
9. Boros, A., Nemes, C., Pankovics, P., Kapusinszky, B., Delwart, E. & Reuter, G. (2013). Genetic characterization of a novel picornavirus in turkeys (Meleagris gallopavo) distinct from turkey galliviruses and megriviruses and distantly related to the members of the genus Avihepatovirus. J Gen Virol 94, 1496-1509.
10. Dacheux, L., Cervantes-Gonzalez, M., Guigon, G., Thiberge, J. M., Vandenbogaert, M., Maufrais, C., Caro, V. & Bourhy, H. (2014). A preliminary study of viral metagenomics of French bat species in contact with humans: identification of new mammalian viruses. PLoS ONE 9, e87194.
11. Dayaram, A., Potter, K. A., Moline, A. B., Rosenstein, D. D., Marinov, M., Thomas, J. E., Breitbart, M., Rosario, K., Argüello-Astorga, G. R. & Varsani, A. (2013). High global diversity of cycloviruses amongst dragonflies. J Gen Virol 94, 1827-1840.
12. Delwart, E. (2013). A roadmap to the human virome. PLoS Pathog 9, e1003146.
13. Delwart, E. & Li, L. (2012). Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes. Virus Res 164, 114-121.
14. Donaldson, E. F., Haskew, A. N., Gates, J. E., Huynh, J., Moore, C. J. & Frieman, M. B. (2010). Metagenomic analysis of the viromes of three North American bat species: viral diversity among different bat species that share a common habitat. J Virol 84, 13004-13018.
15. Dubey, S., Antonin, M., Denys, C. & Vogel, P. (2007). Use of phylogeny to resolve the taxonomy of the widespread and highly polymorphic African giant shrews (Crocidura olivieri group, Crocidurinae, Mammalia). Zoology (Jena) 110, 48-57.
16. Dürrwald, R., Kolodziejek, J., Weissenböck, H. & Nowotny, N. (2014). The bicolored white-toothed shrew Crocidura leucodon (HERMANN 1780) is an indigenous host of mammalian Borna disease virus. PLoS ONE 9, e93659.
17. Esposito, S., Rahamat-Langendoen, J., Ascolese, B., Senatore, L., Castellazzi, L. & Niesters, H. G. (2014). Pediatric parechovirus infections. J Clin Virol 60, 84-89.
18. Firth, C. & Lipkin, W. I. (2013). The genomics of emerging pathogens. Annu Rev Genomics Hum Genet 14, 281-300.
19. Ge, X., Li, J., Peng, C., Wu, L., Yang, X., Wu, Y., Zhang, Y. & Shi, Z. (2011). Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 92, 2646-2653.
20. Ge, X., Li, Y., Yang, X., Zhang, H., Zhou, P., Zhang, Y. & Shi, Z. (2012). Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J Virol 86, 4620-4630.
21. Goodfellow, I. (2011). The genome-linked protein VPg of vertebrate viruses-a multifaceted protein. Curr Opin Virol 1, 355-362.
22. Gorbalenya, A. E., Donchenko, A. P., Blinov, V. M. & Koonin, E. V. (1989). Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases. A distinct protein superfamily with a common structural fold. FEBS Lett 243, 103-114.
23. Guo, W. P., Lin, X. D., Wang, W., Tian, J. H., Cong, M. L., Zhang, H. L., Wang, M. R., Zhou, R. H., Wang, J. B. & other authors (2013). Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog 9, e1003159.
24. Handley, S. A., Thackray, L. B., Zhao, G., Presti, R., Miller, A. D., Droit, L., Abbink, P., Maxfield, L. F., Kambal, A. & other authors (2012). Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151, 253-266.
25. Hilbe, M., Herrsche, R., Kolodziejek, J., Nowotny, N., Zlinszky, K. & Ehrensperger, F. (2006). Shrews as reservoir hosts of borna disease virus. Emerg Infect Dis 12, 675-677.
26. Honkavuori, K. S., Shivaprasad, H. L., Briese, T., Street, C., Hirschberg, D. L., Hutchison, S. K. & Lipkin, W. I. (2011). Novel picornavirus in Turkey poults with hepatitis, California, USA. Emerg Infect Dis 17, 480-487.
27. Huson, D. H., Auch, A. F., Qi, J. & Schuster, S. C. (2007). MEGAN analysis of metagenomic data. Genome Res 17, 377-386.
28. Joffret, M. L., Bouchier, C., Grandadam, M., Zeller, H., Maufrais, C., Bourhy, H., Despres, P., Delpeyroux, F. & Dacheux, L. (2013). Genomic characterization of Sebokele virus 1 (SEBV1) reveals a new candidate species among the genus Parechovirus. J Gen Virol 94, 1547-1553.
29. Kamer, G. & Argos, P. (1984). Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res 12, 7269-7282.
30. Kapoor, A., Victoria, J., Simmonds, P., Slikas, E., Chieochansin, T., Naeem, A., Shaukat, S., Sharif, S., Alam, M. M. & other authors (2008a). A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc Natl Acad Sci U S A 105, 20482-20487.
31. Kapoor, A., Victoria, J., Simmonds, P., Wang, C., Shafer, R. W., Nims, R., Nielsen, O. & Delwart, E. (2008b). A highly divergent picornavirus in a marine mammal. J Virol 82, 311-320.
32. Kapoor, A., Simmonds, P., Lipkin, W. I., Zaidi, S. & Delwart, E. (2010). Use of nucleotide composition analysis to infer hosts for three novel picorna-like viruses. J Virol 84, 10322-10328.
33. King, A. M., Adams, M. J., Lefkowitz, E. J. & Carstens, E. B. (2012). Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier Academic Press.
34. Le Gall, O., Christian, P., Fauquet, C. M., King, A. M., Knowles, N. J., Nakashima, N., Stanway, G. & Gorbalenya, A. E. (2008). Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T53 virion architecture. Arch Virol 153, 715-727.
35. Li, Z., Yu, M., Zhang, H., Wang, H. Y. & Wang, L. F. (2005). Improved rapid amplification of cDNA ends (RACE) for mapping both the 59 and 39 terminal sequences of paramyxovirus genomes. J Virol Methods 130, 154-156.
36. Li, L., Victoria, J., Kapoor, A., Blinkova, O., Wang, C., Babrzadeh, F., Mason, C. J., Pandey, P., Triki, H. & other authors (2009). A novel picornavirus associated with gastroenteritis. J Virol 83, 12002-12006.
37. Li, L., Kapoor, A., Slikas, B., Bamidele, O. S., Wang, C., Shaukat, S., Masroor, M. A., Wilson, M. L., Ndjango, J. B. & other authors (2010a). Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84, 1674-1682.
38. Li, L., Victoria, J. G., Wang, C., Jones, M., Fellers, G. M., Kunz, T. H. & Delwart, E. (2010b). Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84, 6955-6965.
39. Li, L., Shan, T., Soji, O. B., Alam, M. M., Kunz, T. H., Zaidi, S. Z. & Delwart, E. (2011a). Possible cross-species transmission of circoviruses and cycloviruses among farm animals. J Gen Virol 92, 768-772.
40. Li, L., Shan, T., Wang, C., Côté, C., Kolman, J., Onions, D., Gulland, F. M. & Delwart, E. (2011b). The fecal viral flora of California sea lions. J Virol 85, 9909-9917.
41. Lim, E. S., Cao, S., Holtz, L. R., Antonio, M., Stine, O. C. & Wang, D. (2014). Discovery of rosavirus 2, a novel variant of a rodentassociated picornavirus, in children from The Gambia. Virology 454-455, 25-33.
42. Lole, K. S., Bollinger, R. C., Paranjape, R. S., Gadkari, D., Kulkarni, S. S., Novak, N. G., Ingersoll, R., Sheppard, H. W. & Ray, S. C. (1999). Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73, 152-160.
43. Luke, G. A., de Felipe, P., Lukashev, A., Kallioinen, S. E., Bruno, E. A. & Ryan, M. D. (2008). Occurrence, function and evolutionary origins of '2A-like' sequences in virus genomes. J Gen Virol 89, 1036-1042.
44. Lysholm, F., Wetterbom, A., Lindau, C., Darban, H., Bjerkner, A., Fahlander, K., Lindberg, A. M., Persson, B., Allander, T. & Andersson, B. (2012). Characterization of the viral microbiome in patients with severe lower respiratory tract infections, using metagenomic sequencing. PLoS ONE 7, e30875.
45. Malboeuf, C. M., Yang, X., Charlebois, P., Qu, J., Berlin, A. M., Casali, M., Pesko, K. N., Boutwell, C. L., DeVincenzo, J. P. & other authors (2013). Complete viral RNA genome sequencing of ultra-low copy samples by sequence-independent amplification. Nucleic Acids Res 41, e13.
46. Meerburg, B. G., Singleton, G. R. & Kijlstra, A. (2009). Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35, 221-270.
47. Mokili, J. L., Rohwer, F. & Dutilh, B. E. (2012). Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2, 63-77.
48. Morse, S. S., Mazet, J. A., Woolhouse, M., Parrish, C. R., Carroll, D., Karesh, W. B., Zambrana-Torrelio, C., Lipkin, W. I. & Daszak, P. (2012). Prediction and prevention of the next pandemic zoonosis. Lancet 380, 1956-1965.
49. Nakashima, N. & Uchiumi, T. (2009). Functional analysis of structural motifs in dicistroviruses. Virus Res 139, 137-147.
50. Ng, T. F., Marine, R., Wang, C., Simmonds, P., Kapusinszky, B., Bodhidatta, L., Oderinde, B. S., Wommack, K. E. & Delwart, E. (2012). High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage. J Virol 86, 12161-12175.
51. Ng, T. F., Mesquita, J. R., Nascimento, M. S., Kondov, N. O., Wong, W., Reuter, G., Knowles, N. J., Vega, E., Esona, M. D. & other authors (2014). Feline fecal virome reveals novel and prevalent enteric viruses. Vet Microbiol 171, 102-111.
52. Niklasson, B., Kinnunen, L., Hörnfeldt, B., Hörling, J., Benemar, C., Hedlund, K. O., Matskova, L., Hyypiä, T. & Winberg, G. (1999). A new picornavirus isolated from bank voles (Clethrionomys glareolus). Virology 255, 86-93.
53. Padilla-Rodriguez, M., Rosario, K. & Breitbart, M. (2013). Novel cyclovirus discovered in the Florida woods cockroach Eurycotis floridana (Walker). Arch Virol 158, 1389-1392.
54. Phan, T. G., Kapusinszky, B., Wang, C., Rose, R. K., Lipton, H. L. & Delwart, E. L. (2011). The fecal viral flora of wild rodents. PLoS Pathog 7, e1002218.
55. Phan, T. G., Vo, N. P., Boros, Á., Pankovics, P., Reuter, G., Li, O. T., Wang, C., Deng, X., Poon, L. L. & Delwart, E. (2013a). The viruses of wild pigeon droppings. PLoS One 8, e72787.
56. Phan, T. G., Vo, N. P., Simmonds, P., Samayoa, E., Naccache, S., Chiu, C. Y. & Delwart, E. (2013b). Rosavirus: the prototype of a proposed new genus of the Picornaviridae family. Virus Genes 47, 556-558.
57. Phan, T. G., Luchsinger, V., Avendaño, L. F., Deng, X. & Delwart, E. (2014). Cyclovirus in nasopharyngeal aspirates of Chilean children with respiratory infections. J Gen Virol 95, 922-927.
58. Reuter, G., Pankovics, P., Knowles, N. J. & Boros, Á. (2012). Two closely related novel picornaviruses in cattle and sheep in Hungary from 2008 to 2009, proposed as members of a new genus in the family Picornaviridae. J Virol 86, 13295-13302.
59. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. (2012). MrBayes 3. 2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61, 539-542.
60. Rosario, K., Marinov, M., Stainton, D., Kraberger, S., Wiltshire, E. J., Collings, D. A., Walters, M., Martin, D. P., Breitbart, M. & Varsani, A. (2011). Dragonfly cyclovirus, a novel single-stranded DNA virus discovered in dragonflies (Odonata: Anisoptera). J Gen Virol 92, 1302-1308.
61. Rosario, K., Duffy, S. & Breitbart, M. (2012). A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157, 1851-1871.
62. Sasaki, M., Muleya, W., Ishii, A., Orba, Y., Hang'ombe, B. M., Mweene, A. S., Moonga, L., Thomas, Y., Kimura, T. & Sawa, H. (2014). Molecular epidemiology of paramyxoviruses in Zambian wild rodents and shrews. J Gen Virol 95, 325-330.
63. Sauvage, V., Ar Gouilh, M., Cheval, J., Muth, E., Pariente, K., Burguiere, A., Caro, V., Manuguerra, J. C. & Eloit, M. (2012). A member of a new Picornaviridae genus is shed in pig feces. J Virol 86, 10036-10046.
64. Shan, T., Li, L., Simmonds, P., Wang, C., Moeser, A. & Delwart, E. (2011). The fecal virome of pigs on a high-density farm. J Virol 85, 11697-11708.
65. Shirai, Y., Takao, Y., Mizumoto, H., Tomaru, Y., Honda, D. & Nagasaki, K. (2006). Genomic and phylogenetic analysis of a singlestranded RNA virus infecting Rhizosolenia setigera (Stramenopiles: Bacillariophyceae). J Mar Biol Assoc U K 86, 475-483.
66. Simmonds, P. (2012). SSE: a nucleotide and amino acid sequence analysis platform. BMC Res Notes 5, 50.
67. Smith, I. & Wang, L. F. (2013). Bats and their virome: an important source of emerging viruses capable of infecting humans. Curr Opin Virol 3, 84-91.
68. Smits, S. L., Raj, V. S., Oduber, M. D., Schapendonk, C. M., Bodewes, R., Provacia, L., Stittelaar, K. J., Osterhaus, A. D. & Haagmans, B. L. (2013a). Metagenomic analysis of the ferret fecal viral flora. PLoS One 8, e71595.
69. Smits, S. L., Zijlstra, E. E., van Hellemond, J. J., Schapendonk, C. M., Bodewes, R., Schürch, A. C., Haagmans, B. L. & Osterhaus, A. D. (2013b). Novel cyclovirus in human cerebrospinal fluid, Malawi, 2010-2011. Emerg Infect Dis 19, no. 9.
70. Sweeney, T. R., Cisnetto, V., Bose, D., Bailey, M., Wilson, J. R., Zhang, X., Belsham, G. J. & Curry, S. (2010). Foot-and-mouth disease virus 2C is a hexameric AAA+ protein with a coordinated ATP hydrolysis mechanism. J Biol Chem 285, 24347-24359.
71. Takao, Y., Mise, K., Nagasaki, K., Okuno, T. & Honda, D. (2006). Complete nucleotide sequence and genome organization of a singlestranded RNA virus infecting the marine fungoid protist Schizochytrium sp. J Gen Virol 87, 723-733.
72. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6. 0. Mol Biol Evol 30, 2725-2729.
73. Tan, V., van Doorn, H. R., Nghia, H. D., Chau, T. T., Tu, T. P., de Vries, M., Canuti, M., Deijs, M., Jebbink, M. F. & other authors (2013). Identification of a new cyclovirus in cerebrospinal fluid of patients with acute central nervous system infections. MBio 4, e00231-e13.
74. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
75. Trujillo-Ortiz, A., Hernandez-Walls, R. & Perez-Osuna, S. (2004). RAFisher2cda: canonical discriminant analysis. http://www. mathworks. co. uk/matlabcentral/fileexchange/4836-rafisher2cda.
76. van den Brand, J. M., van Leeuwen, M., Schapendonk, C. M., Simon, J. H., Haagmans, B. L., Osterhaus, A. D. & Smits, S. L. (2012). Metagenomic analysis of the viral flora of pine marten and European badger feces. J Virol 86, 2360-2365.
77. Williams, C. H., Panayiotou, M., Girling, G. D., Peard, C. I., Oikarinen, S., Hyöty, H. & Stanway, G. (2009). Evolution and conservation in human parechovirus genomes. J Gen Virol 90, 1702-1712.
78. Wilson, D. E. & Reeder, D. M. (2011). Class Mammalia Linnaeus, 1758. Zootaxa 3148, 56-60.
79. Witkowski, P. T., Klempa, B., Ithete, N. L., Auste, B., Mfune, J. K., Hoveka, J., Matthee, S., Preiser, W. & Kruger, D. H. (2014). Hantaviruses in Africa. Virus Res 187, 34-42.
80. Woo, P. C., Lau, S. K., Huang, Y., Lam, C. S., Poon, R. W., Tsoi, H. W., Lee, P., Tse, H., Chan, A. S. & other authors (2010). Comparative analysis of six genome sequences of three novel picornaviruses, turdiviruses 1, 2 and 3, in dead wild birds, and proposal of two novel genera, Orthoturdivirus and Paraturdivirus, in the family Picornaviridae. J Gen Virol 91, 2433-2448.
81. Woo, P. C., Lau, S. K., Choi, G. K., Huang, Y., Teng, J. L., Tsoi, H. W., Tse, H., Yeung, M. L., Chan, K. H. & other authors (2012). Natural occurrence and characterization of two internal ribosome entry site elements in a novel virus, canine picodicistrovirus, in the picornavirus-like superfamily. J Virol 86, 2797-2808.
82. Wu, Z., Ren, X., Yang, L., Hu, Y., Yang, J., He, G., Zhang, J., Dong, J., Sun, L. & other authors (2012). Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J Virol 86, 10999-11012.
83. Yanagihara, R., Gu, S. H., Arai, S., Kang, H. J. & Song, J. W. (2014). Hantaviruses: rediscovery and new beginnings. Virus Res 187, 6-14.
84. Yozwiak, N. L., Skewes-Cox, P., Gordon, A., Saborio, S., Kuan, G., Balmaseda, A., Ganem, D., Harris, E. & DeRisi, J. L. (2010). Human enterovirus 109: a novel interspecies recombinant enterovirus isolated from a case of acute pediatric respiratory illness in Nicaragua. J Virol 84, 9047-9058.
85. Yu, J. M., Li, X. Y., Ao, Y. Y., Li, L. L., Liu, N., Li, J. S. & Duan, Z. J. (2013). Identification of a novel picornavirus in healthy piglets and seroepidemiological evidence of its presence in humans. PLoS One 8, e70137.
86. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31, 3406-3415.