Bat guano virome: Predominance of dietary viruses from insects and plants plus novel mammalian viruses

Journal of Virology

Volumn 84, Issue 14, 2010, Pages 6955-6965

  Li, Linlin ^a,b   Victoria, Joseph G ^a,b   Wang, Chunlin ^c   Jones, Morris ^d   Fellers, Gary M ^e   Kunz, Thomas H ^f   Delwart, Eric ^a,b  

^a BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DAVID GRANT MEDICAL CENTER   (United States)

^e U S GEOLOGICAL SURVEY   (United States)

^f Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BAT; DENSOVIRUS; DICISTROVIRIDAE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC ANALYSIS; INSECT VIRUS; MAMMAL; NODAVIRUS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT VIRUS; PRIORITY JOURNAL; VIRUS GENE;

ANIMALS; CALIFORNIA; CHIROPTERA; DIET; DISEASE OUTBREAKS; DISEASE RESERVOIRS; FECES; GENOME, VIRAL; HUMANS; INSECTS; MAMMALS; METAGENOMICS; PHYLOGENY; PLANTS; SEQUENCE ANALYSIS, DNA; TEXAS; VIRUS DISEASES; VIRUSES; ZOONOSES;

ADENOVIRIDAE; ANIMALIA; ASTROVIRIDAE; CIRCOVIRIDAE; CORONAVIRIDAE; DENSOVIRINAE; DICISTROVIRIDAE; EUKARYOTA; FUNGI; HEXAPODA; LUTEOVIRIDAE; MAMMALIA; NODAVIRIDAE; PARTITIVIRIDAE; PARVOVIRIDAE; PICORNAVIRIDAE; POXVIRIDAE; SOBEMOVIRUS; TETRAVIRIDAE; TYMOVIRIDAE;

EID: 77953786835     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00501-10     Document Type: Article

References (68)

1. Allander, T., S. U. Emerson, R. E. Engle, R. H. Purcell, and J. Bukh. 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.
2. Blehert, D. S., A. C. Hicks, M. Behr, C. U. Meteyer, B. M. Berlowski-Zier, E. L. Buckles, J. T. Coleman, S. R. Darling, A. Gargas, R. Niver, J. C. Okoniewski, R. J. Rudd, and W. B. Stone. 2009. Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227.
3. Breitbart, M., M. Haynes, S. Kelley, F. Angly, R. A. Edwards, B. Felts, J. M. Mahaffy, J. Mueller, J. Nulton, S. Rayhawk, B. Rodriguez-Brito, P. Salamon, and F. Rohwer. 2008. Viral diversity and dynamics in an infant gut. Res. Microbiol. 159:367-373.
4. Breitbart, M., I. Hewson, B. Felts, J. M. Mahaffy, J. Nulton, P. Salamon, and F. Rohwer. 2003. Metagenomic analyses of an uncultured viral community from human feces. J. Bacteriol. 185:6220-6223. (Pubitemid 37248478)
5. Breitbart, M., and F. Rohwer. 2005. Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing. Biotechniques 39:729-736.
6. Calisher, C. H., J. E. Childs, H. E. Field, K. V. Holmes, and T. Schountz. 2006. Bats: important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 19:531-545.
7. Cann, A. J., S. E. Fandrich, and S. Heaphy. 2005. Analysis of the virus population present in equine faeces indicates the presence of hundreds of uncharacterized virus genomes. Virus Genes 30:151-156.
8. Chu, D. K., L. L. Poon, Y. Guan, and J. S. Peiris. 2008. Novel astroviruses in insectivorous bats. J. Virol. 82:9107-9114.
9. Chua, K. B., G. Crameri, A. Hyatt, M. Yu, M. R. Tompang, J. Rosli, J. McEachern, S. Crameri, V. Kumarasamy, B. T. Eaton, and L. F. Wang. 2007. A previously unknown reovirus of bat origin is associated with an acute respiratory disease in humans. Proc. Natl. Acad. Sci. U. S. A. 104:11424-11429.
10. Crameri, G., S. Todd, S. Grimley, J. A. McEachern, G. A. Marsh, C. Smith, M. Tachedjian, C. De Jong, E. R. Virtue, M. Yu, D. Bulach, J. P. Liu, W. P. Michalski, D. Middleton, H. E. Field, and L. F. Wang. 2009. Establishment, immortalisation and characterisation of pteropid bat cell lines. PLoS One 4:e8266.
11. Delwart, E. L. 2007. Viral metagenomics. Rev. Med. Virol. 17:115-131.
12. de Miranda, J. R., M. Drebot, S. Tyler, M. Shen, C. E. Cameron, D. B. Stoltz, and S. M. Camazine. 2004. Complete nucleotide sequence of Kashmir bee virus and comparison with acute bee paralysis virus. J. Gen. Virol. 85:2263-2270.
13. Drexler, J. F., V. M. Corman, F. Gloza-Rausch, A. Seebens, A. Annan, A. Ipsen, T. Kruppa, M. A. Muller, E. K. Kalko, Y. Adu-Sarkodie, S. Oppong, and C. Drosten. 2009. Henipavirus RNA in African bats. PLoS One 4:e6367.
14. Feng, H., M. Shuda, Y. Chang, and P. S. Moore. 2008. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 319:1096-1100. (Pubitemid 351300792)
15. Finkbeiner, S. R., A. F. Allred, P. I. Tarr, E. J. Klein, C. D. Kirkwood, and D. Wang. 2008. Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS Pathog. 4:e1000011.
16. Finkbeiner, S. R., L. R. Holtz, Y. Jiang, P. Rajendran, C. J. Franz, G. Zhao, G. Kang, and D. Wang. 2009. Human stool contains a previously unrecognized diversity of novel astroviruses. Virol. J. 6:161.
17. Gao, G., M. R. Alvira, S. Somanathan, Y. Lu, L. H. Vandenberghe, J. J. Rux, R. Calcedo, J. Sanmiguel, Z. Abbas, and J. M. Wilson. 2003. Adeno-associated viruses undergo substantial evolution in primates during natural infections. Proc. Natl. Acad. Sci. U. S. A. 100:6081-6086.
18. Gaynor, A. M., M. D. Nissen, D. M. Whiley, I. M. Mackay, S. B. Lambert, G. Wu, D. C. Brennan, G. A. Storch, T. P. Sloots, and D. Wang. 2007. Identification of a novel polyomavirus from patients with acute respiratory tract infections. PLoS Pathog. 3:e64.
19. Govan, V. A., N. Leat, M. Allsopp, and S. Davison. 2000. Analysis of the complete genome sequence of acute bee paralysis virus shows that it belongs to the novel group of insect-infecting RNA viruses. Virology 277:457-463.
20. Greninger, A. L., C. Runckel, C. Y. Chiu, T. Haggerty, J. Parsonnet, D. Ganem, and J. L. DeRisi. 2009. The complete genome of klassevirus - a novel picornavirus in pediatric stool. Virol. J. 6:82.
21. Holtz, L. R., S. R. Finkbeiner, G. Zhao, C. D. Kirkwood, R. Girones, J. M. Pipas, and D. Wang. 2009. Klassevirus 1, a previously undescribed member of the family Picornaviridae, is globally widespread. Virol. J. 6:86.
22. Jones, M. S., A. Kapoor, V. V. Lukashov, P. Simmonds, F. Hecht, and E. Delwart. 2005. New DNA viruses identified in patients with acute viral infection syndrome. J. Virol. 79:8230-8236.
23. Kapoor, A., L. Li, J. Victoria, B. Oderinde, C. Mason, P. Pandey, S. Z. Zaidi, and E. Delwart. 2009. Multiple novel astrovirus species in human stool. J. Gen. Virol. 90:2965-2972.
24. Kapoor, A., E. Slikas, P. Simmonds, T. Chieochansin, A. Naeem, S. Shaukat, M. M. Alam, S. Sharif, M. Angez, S. Zaidi, and E. Delwart. 2009. A newly identified bocavirus species in human stool. J. Infect. Dis. 199:196-200.
25. Kapoor, A., J. Victoria, P. Simmonds, E. Slikas, T. Chieochansin, A. Naeem, S. Shaukat, S. Sharif, M. M. Alam, M. Angez, C. Wang, R. W. Shafer, S. Zaidi, and E. Delwart. 2008. A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc. Natl. Acad. Sci. U. S. A. 105:20482-20487.
26. Khamrin, P., N. Maneekarn, A. Kongkaew, S. Kongkaew, S. Okitsu, and H. Ushijima. 2009. Porcine kobuvirus in piglets, Thailand. Emerg. Infect. Dis. 15:2075-2076.
27. Khamrin, P., N. Maneekarn, S. Peerakome, S. Okitsu, M. Mizuguchi, and H. Ushijima. 2008. Bovine kobuviruses from cattle with diarrhea. Emerg. Infect. Dis. 14:985-986.
28. Kristensen, D. M., A. R. Mushegian, V. V. Dolja, and E. V. Koonin. 2010. New dimensions of the virus world discovered through metagenomics. Trends Microbiol. 18:11-19.
29. Kumar, S., M. Nei, J. Dudley, and K. Tamura. 2008. MEGA: a biologistcentric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform. 9:299-306. (Pubitemid 351890826)
30. Kunz, T. H., and M. B. Fenton. 2003. Bat Ecology. University of Chicago Press, Chicago, IL.
31. Kuzmin, I. V., M. Niezgoda, R. Franka, B. Agwanda, W. Markotter, J. C. Beagley, O. Y. Urazova, R. F. Breiman, and C. E. Rupprecht. 2008. Possible emergence of West Caucasian bat virus in Africa. Emerg. Infect. Dis. 14:1887-1889.
32. Lau, S. K., K. S. Li, Y. Huang, C.-T. Shek, H. Tse, M. Wang, G. K. Choi, H. Xu, C. S. Lam, R. Guo, K.-H. Chan, B.-J. Zheng, P. C. Woo, and K.-Y. Yuen. 2010. Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. J. Virol. 84:2808-2819.
33. Li, L., A. Kapoor, B. Slikas, O. S. Bamidele, C. Wang, S. Shaukat, M. A. Masroor, M. L. Wilson, J. B. Ndjango, M. Peeters, N. D. Gross-Camp, M. N. Muller, B. H. Hahn, N. D. Wolfe, H. Triki, J. Bartkus, S. Z. Zaidi, and E. Delwart. 2010. Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J. Virol. 84:1674-1682.
34. Li, L., J. Victoria, A. Kapoor, O. Blinkova, C. Wang, F. Babrzadeh, C. J. Mason, P. Pandey, H. Triki, O. Bahri, B. S. Oderinde, M. M. Baba, D. N. Bukbuk, J. M. Besser, J. M. Bartkus, and E. L. Delwart. 2009. A novel picornavirus associated with gastroenteritis. J. Virol. 83:12002-12006.
35. Li, Y., X. Ge, H. Zhang, P. Zhou, Y. Zhu, Y. Zhang, J. Yuan, L.-F. Wang, and Z. Shi. 2010. Host range, prevalence, and genetic diversity of adenoviruses in bats. J. Virol. 84:3889-3897.
36. Liu, C., J. Zhang, F. Yi, J. Wang, X. Wang, H. Jiang, J. Xu, and Y. Hu. 2006. Isolation and RNA1 nucleotide sequence determination of a new insect nodavirus from Pieris rapae larvae in Wuhan city, China. Virus Res. 120:28-35. (Pubitemid 43947298)
37. Luby, S. P., E. S. Gurley, and M. J. Hossain. 2009. Transmission of human infection with Nipah virus. Clin. Infect. Dis. 49:1743-1748.
38. Mackenzie, J. S. 2005. Emerging zoonotic encephalitis viruses: lessons from Southeast Asia and Oceania. J. Neurovirol. 11:434-440.
39. Maeda, K., E. Hondo, J. Terakawa, Y. Kiso, N. Nakaichi, D. Endoh, K. Sakai, S. Morikawa, and T. Mizutani. 2008. Isolation of novel adenovirus from fruit bat (Pteropus dasymallus yayeyamae). Emerg. Infect. Dis. 14:347-349.
40. McKnight, C. A., A. G. Wise, R. K. Maes, C. Howe, A. Rector, M. Van Ranst, and M. Kiupel. 2006. Papillomavirus-associated basosquamous carcinoma in an Egyptian fruit bat (Rousettus aegyptiacus). J. Zoo Wildl. Med. 37:193-196.
41. Messenger, S. L., C. E. Rupprecht, and J. S. Smith. 2003. Bats, emerging virus infections, and the rabies paradigm, p. 622-679. In T. H. Kunz and M. B. Fenton (ed.), Bat ecology. University of Chicago Press, Chicago, IL.
42. Misra, V., T. Dumonceaux, J. Dubois, C. Willis, S. Nadin-Davis, A. Severini, A. Wandeler, R. Lindsay, and H. Artsob. 2009. Detection of polyoma and corona viruses in bats of Canada. J. Gen. Virol. 90:2015-2022.
43. Monroe, S., M. Carter, J. Hermann, D. Mitchell, and A. Sanchez-Fauquier. 2005. Astroviridae, p. 859-864. In C. Fauquet, M. Mayo, J. Maniloff, U. Desselberger, and L. Ball (ed.), Virus taxonomy: eighth report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
44. Mori, S., L. Wang, T. Takeuchi, and T. Kanda. 2004. Two novel adeno-associated viruses from cynomolgus monkey: pseudotyping characterization of capsid protein. Virology 330:375-383.
45. Nakamura, S., C. S. Yang, N. Sakon, M. Ueda, T. Tougan, A. Yamashita, N. Goto, K. Takahashi, T. Yasunaga, K. Ikuta, T. Mizutani, Y. Okamoto, M. Tagami, R. Morita, N. Maeda, J. Kawai, Y. Hayashizaki, Y. Nagai, T. Horii, T. Iida, and T. Nakaya. 2009. Direct metagenomic detection of viral pathogens in nasal and fecal specimens using an unbiased high-throughput sequencing approach. PLoS One 4:e4219.
46. Omatsu, T., S. Watanabe, H. Akashi, and Y. Yoshikawa. 2007. Biological characters of bats in relation to natural reservoir of emerging viruses. Comp. Immunol. Microbiol. Infect. Dis. 30:357-374.
47. Quan, P. L., S. Junglen, A. Tashmukhamedova, S. Conlan, S. K. Hutchison, A. Kurth, H. Ellerbrok, M. Egholm, T. Briese, F. H. Leendertz, and W. I. Lipkin. 2010. Moussa virus: a new member of the Rhabdoviridae family isolated from Culex decens mosquitoes in Cote d'Ivoire. Virus Res. 147:17-24.
48. Reuter, G., A. Boldizsar, and P. Pankovics. 2009. Complete nucleotide and amino acid sequences and genetic organization of porcine kobuvirus, a member of a new species in the genus Kobuvirus, family Picornaviridae. Arch. Virol. 154:101-108.
49. Rivera, R., H. H. Nollens, S. Venn-Watson, F. M. Gulland, and J. F. Wellehan, Jr. 2010. Characterization of phylogenetically diverse astroviruses of marine mammals. J. Gen. Virol. 91:166-173.
50. Rosario, K., S. Duffy, and M. Breitbart. 2009. Diverse circovirus-like genome architectures revealed by environmental metagenomics. J. Gen. Virol. 90:2418-2424.
51. Roy, S., L. H. Vandenberghe, S. Kryazhimskiy, R. Grant, R. Calcedo, X. Yuan, M. Keough, A. Sandhu, Q. Wang, C. A. Medina-Jaszek, J. B. Plotkin, and J. M. Wilson. 2009. Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog. 5:e1000503.
52. Schmidt, M., H. Katano, I. Bossis, and J. A. Chiorini. 2004. Cloning and characterization of a bovine adeno-associated virus. J. Virol. 78:6509-6516.
53. Schmidt, M., A. Voutetakis, S. Afione, C. Zheng, D. Mandikian, and J. A. Chiorini. 2008. Adeno-associated virus type 12 (AAV12): a novel AAV serotype with sialic acid-and heparan sulfate proteoglycan-independent transduction activity. J. Virol. 82:1399-1406.
54. Simmons, N. B. 2005. Chiropttera, p. 312-529. In D. E. Wilson and D. M. Reeder (ed.), Mammal species of the world: a taxonomic reference. Smithsonian Institution Press, Washington, DC.
55. Skliris, G. P., J. V. Krondiris, D. C. Sideris, A. P. Shinn, W. G. Starkey, and R. H. Richards. 2001. Phylogenetic and antigenic characterization of new fish nodavirus isolates from Europe and Asia. Virus Res. 75:59-67.
56. Sonntag, M., K. Muhldorfer, S. Speck, G. Wibbelt, and A. Kurth. 2009. New adenovirus in bats, Germany. Emerg. Infect. Dis. 15:2052-2055.
57. Tattersall, P., M. Bergoin, M. Bloom, K. Brown, R. Linden, and P. Tijssen. 2005. Paroviridae, p. 353-369. In C. Fauquet, M. Mayo, J. Maniloff, U. Desselberger, and L. Ball (ed.), Virus taxonomy: eighth report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
58. Teeling, E. C., M. S. Springer, O. Madsen, P. Bates, S. J. O'Brien, and W. J. Murphy. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580-584.
59. van der Poel, W. H., P. H. Lina, and J. A. Kramps. 2006. Public health awareness of emerging zoonotic viruses of bats: a European perspective. Vector Borne Zoonotic Dis. 6:315-324.
60. Victoria, J. G., A. Kapoor, L. Li, O. Blinkova, B. Slikas, C. Wang, A. Naeem, S. Zaidi, and E. Delwart. 2009. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J. Virol. 83:4642-4651.
61. Wang, L. F., E. Hansson, M. Yu, K. B. Chua, N. Mathe, G. Crameri, B. K. Rima, J. Moreno-Lopez, and B. T. Eaton. 2007. Full-length genome sequence and genetic relationship of two paramyxoviruses isolated from bat and pigs in the Americas. Arch. Virol. 152:1259-1271.
62. Watanabe, S., N. Ueda, K. Iha, J. S. Masangkay, H. Fujii, P. Alviola, T. Mizutani, K. Maeda, D. Yamane, A. Walid, K. Kato, S. Kyuwa, Y. Tohya, Y. Yoshikawa, and H. Akashi. 2009. Detection of a new bat gammaherpesvirus in the Philippines. Virus Genes 39:90-93.
63. Wibbelt, G., S. Speck, and H. Field. 2009. Methods for assessing diseases in bats, p. 775-794. In T. H. Kunz and S. Parsons (ed.), Ecological and behavioral methods for the study of bats. Johns Hopkins University Press, Baltimore, MD.
64. Willner, D., M. Furlan, M. Haynes, R. Schmieder, F. E. Angly, J. Silva, S. Tammadoni, B. Nosrat, D. Conrad, and F. Rohwer. 2009. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS One 4:e7370.
65. Wong, S., S. Lau, P. Woo, and K. Y. Yuen. 2007. Bats as a continuing source of emerging infections in humans. Rev. Med. Virol. 17:67-91.
66. Yamashita, T., M. Ito, Y. Kabashima, H. Tsuzuki, A. Fujiura, and K. Sakae. 2003. Isolation and characterization of a new species of kobuvirus associated with cattle. J. Gen. Virol. 84:3069-3077.
67. Zhang, T., M. Breitbart, W. H. Lee, J. Q. Run, C. L. Wei, S. W. Soh, M. L. Hibberd, E. T. Liu, F. Rohwer, and Y. Ruan. 2006. RNA viral community in human feces: prevalence of plant pathogenic viruses. PLoS Biol. 4:e3.
68. Zhu, H. C., D. K. Chu, W. Liu, B. Q. Dong, S. Y. Zhang, J. X. Zhang, L. F. Li, D. Vijaykrishna, G. J. Smith, H. L. Chen, L. L. Poon, J. S. Peiris, and Y. Guan. 2009. Detection of diverse astroviruses from bats in China. J. Gen. Virol. 90:883-887.