A preliminary study of viral metagenomics of french bat species in contact with humans: Identification of new mammalian viruses

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Dacheux, Laurent ^a   Cervantes Gonzalez, Minerva ^a   Guigon, Ghislaine ^a   Thiberge, Jean Michel ^a   Vandenbogaert, Mathias ^a   Maufrais, Corinne ^a   Caro, Valérie ^a   Bourhy, Hervé ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CONTIG;

ANIMAL TISSUE; ARTICLE; BACTERIUM; BAT; BORNA DISEASE VIRUS; BRAIN; BUNYAVIRUS; CARCASS; CONTACT EXAMINATION; DNA SEQUENCE; EPTESICUS SEROTINUS; FEMALE; FLAVIVIRUS; FRENCH BAT; FUNGUS; HERPES VIRUS; HYPSUGO SAVII; INSECT; LIVER; LUNG; MALE; METAGENOMICS; MICROBIAL DIVERSITY; MYOTIS MYSTACINUS; MYOTIS NATTERERI; NAIRO VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PICOBIRNAVIRIDAE; PICOBIRNAVIRUS; PIPISTRELLUS PIPISTRELLUS; PLANT; POXVIRUS; REOVIRUS; RETROVIRUS; ROTAVIRUS; VERTEBRATE; VIRUS IDENTIFICATION; ZOONOSIS;

ANIMALS; BORNAVIRIDAE; CHIROPTERA; FEMALE; FRANCE; GAMMARETROVIRUS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; METAGENOME; MOLECULAR SEQUENCE DATA; NAIROVIRUS; PHYLOGENY; RNA, VIRAL; ROTAVIRUS; SEQUENCE ANALYSIS, RNA;

EID: 84900297457     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087194     Document Type: Article

References (87)

1. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev 19: 531-545. (Pubitemid 44134308)
2. Watanabe S, Maeda K, Suzuki K, Ueda N, Iha K, et al. (2010) Novel betaherpesvirus in bats. Emerg Infect Dis 16: 986-988.
3. Mackenzie JS (2005) Emerging zoonotic encephalitis viruses: lessons from Southeast Asia and Oceania. J Neurovirol 11: 434-440.
4. Drexler JF, Corman VM, Muller MA, Maganga GD, Vallo P, et al. (2012) Bats host major mammalian paramyxoviruses. Nat Commun 3: 796.
5. van der Poel WH, Lina PH, Kramps JA (2006) Public health awareness of emerging zoonotic viruses of bats: a European perspective. Vector Borne Zoonotic Dis 6: 315-324. (Pubitemid 46157512)
6. Wong S, Lau S, Woo P, Yuen KY (2007) Bats as a continuing source of emerging infections in humans. Rev Med Virol 17: 67-91. (Pubitemid 46480593)
7. Luby SP, Gurley ES, Hossain MJ (2009) Transmission of human infection with Nipah virus. Clin Infect Dis 49: 1743-1748.
8. Yob JM, Field H, Rashdi AM, Morrissy C, van der Heide B, et al. (2001) Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerg Infect Dis 7: 439-441.
9. Halpin K, Young PL, Field HE, Mackenzie JS (2000) Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81: 1927-1932. (Pubitemid 30599172)
10. Li W, Shi Z, Yu M, Ren W, Smith C, et al. (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310: 676-679. (Pubitemid 41528160)
11. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, et al. (2005) Fruit bats as reservoirs of Ebola virus. Nature 438: 575-576. (Pubitemid 41740557)
12. Towner JS, Amman BR, Sealy TK, Carroll SA, Comer JA, et al. (2009) Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog 5: e1000536.
13. Freuling CM, Beer M, Conraths FJ, Finke S, Hoffmann B, et al. (2011) Novel lyssavirus in Natterer's bat, Germany. Emerg Infect Dis 17: 1519-1522.
14. Davis PL, Bourhy H, Holmes EC (2006) The evolutionary history and dynamics of bat rabies virus. Infect Genet Evol 6: 464-473. (Pubitemid 44542625)
15. Dacheux L, Larrous F, Mailles A, Boisseleau D, Delmas O, et al. (2009) European bat Lyssavirus transmission among cats, Europe. Emerg Infect Dis 15: 280-284.
16. Donaldson EF, Haskew AN, Gates JE, Huynh J, Moore CJ, et al. (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.
17. Ge X, Li Y, Yang X, Zhang H, Zhou P, et al. (2012) Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J Virol 86: 4620-4630.
18. Li L, Victoria JG, Wang C, Jones M, Fellers GM, et al. (2010) Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84: 6955-6965.
19. Tse H, Tsang AK, Tsoi HW, Leung AS, Ho CC, et al. (2012) Identification of a novel bat papillomavirus by metagenomics. PLoS One 7: e43986.
20. Wu Z, Ren X, Yang L, Hu Y, Yang J, et al. (2012) Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J Virol 86: 10999-11012.
21. Baker KS, Leggett RM, Bexfield NH, Alston M, Daly G, et al. (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.
22. He B, Li Z, Yang F, Zheng J, Feng Y, et al. (2013) Virome profiling of bats from myanmar by metagenomic analysis of tissue samples reveals more novel Mammalian viruses. PLoS One 8: e61950.
23. Chu DK, Poon LL, Guan Y, Peiris JS (2008) Novel astroviruses in insectivorous bats. J Virol 82: 9107-9114.
24. Drexler JF, Gloza-Rausch F, Glende J, Corman VM, Muth D, et al. (2010) Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J Virol 84: 11336-11349.
25. Lau SK, Woo PC, Lai KK, Huang Y, Yip CC, et al. (2011) Complete genome analysis of three novel picornaviruses from diverse bat species. J Virol 85: 8819-8828.
26. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, et al. (2005) Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 102: 14040-14045. (Pubitemid 41377699)
27. Poon LL, Chu DK, Chan KH, Wong OK, Ellis TM, et al. (2005) Identification of a novel coronavirus in bats. J Virol 79: 2001-2009. (Pubitemid 40204557)
28. Zhu HC, Chu DK, Liu W, Dong BQ, Zhang SY, et al. (2009) Detection of diverse astroviruses from bats in China. J Gen Virol 90: 883-887.
29. Bourhy H, Rollin PE, Vincent J, Sureau P (1989) Comparative field evaluation of the fluorescent-antibody test, virus isolation from tissue culture, and enzyme immunodiagnosis for rapid laboratory diagnosis of rabies. J Clin Microbiol 27: 519-523. (Pubitemid 19072364)
30. Dacheux L, Berthet N, Dissard G, Holmes EC, Delmas O, et al. (2010) Application of broad-spectrum resequencing microarray for genotyping rhabdoviruses. J Virol 84: 9557-9574.
31. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
32. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829. (Pubitemid 351645072)
33. Joffret ML, Bouchier C, Grandadam M, Zeller H, Maufrais C, et al. (2013) Genomic characterization of Sebokele virus 1 (SEBV1) reveals a new candidate species among the genus Parechovirus. J Gen Virol.
34. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882. (Pubitemid 28022245)
35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. (Pubitemid 350162903)
36. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599. (Pubitemid 47236692)
37. Elliott RM, Bouloy M, Calisher CH, Goldbach R, Moyer JT, et al. (2000) Family Bunyaviridae. In: van Regenmortel MHV, Fauquet CM, Bishop DHL, editors. Virus Taxonomy: Seventh report of the International Committee on Taxonomy of Viruses. San Diego: Academic Press. 599-621.
38. Nichol ST (2001) Bunyaviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al., editors. Fields Virology. Philadelphia: Lippincott Williams and Wilkins. 1603-1634.
39. Walter CT, Bento DF, Alonso AG, Barr JN (2011) Amino acid changes within the Bunyamwera virus nucleocapsid protein differentially affect the mRNA transcription and RNA replication activities of assembled ribonucleoprotein templates. J Gen Virol 92: 80-84.
40. Schmaljohn CS, Nichol ST (2007) Bunyaviridae. In: Knipe DM, Howley PM, editors. Fields Virology. 5 ed. Philadelphia: Lippincott, Williams and Wilkins. 1741-1790.
41. Ghosh S, Adachi N, Gatheru Z, Nyangao J, Yamamoto D, et al. (2011) Whole-genome analysis reveals the complex evolutionary dynamics of Kenyan G2P[4] human rotavirus strains. J Gen Virol 92: 2201-2208.
42. Estes MK, Kapikian AZ (2007) Rotaviruses. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA et al., editors. Fields Virology. 5 ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins. 1917-1974.
43. Martella V, Banyai K, Matthijnssens J, Buonavoglia C, Ciarlet M (2010) Zoonotic aspects of rotaviruses. Vet Microbiol 140: 246-255.
44. He B, Yang F, Yang W, Zhang Y, Feng Y, et al. (2013) Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J Virol.
45. Coffin JM, Hughes SH, Varmus HE (1997) Retroviruses. NY: Cold Spring Harbor Laboratory Press.
46. Weiss RA (2006) The discovery of endogenous retroviruses. Retrovirology 3: 67.
47. Gifford R, Tristem M (2003) The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26: 291-315.
48. Lipkin WI, Briese T (2007) Bornaviridae. In: Knipe DM, Howley PM, editors. Fields Virology. 5th ed. Philadelphia: Wolters Kluwer/Lippincott Williams and Wilkins. 1449-1496.
49. Rott R, Becht H (1995) Natural and experimental Borna disease in animals. Curr Top Microbiol Immunol 190: 17-30.
50. Kistler AL, Gancz A, Clubb S, Skewes-Cox P, Fischer K, et al. (2008) Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent. Virol J 5: 88.
51. Honkavuori KS, Shivaprasad HL, Williams BL, Quan PL, Hornig M, et al. (2008) Novel borna virus in psittacine birds with proventricular dilatation disease. Emerg Infect Dis 14: 1883-1886.
52. Briese T, Schneemann A, Lewis AJ, Park YS, Kim S, et al. (1994) Genomic organization of Borna disease virus. Proc Natl Acad Sci U S A 91: 4362-4366. (Pubitemid 24143433)
53. de la Torre JC, Carbone KM, Lipkin WI (1990) Molecular characterization of the Borna disease agent. Virology 179: 853-856.
54. Belyi VA, Levine AJ, Skalka AM (2010) Unexpected inheritance: multiple integrations of ancient bornavirus and ebolavirus/marburgvirus sequences in vertebrate genomes. PLoS Pathog 6: e1001030.
55. Horie M, Honda T, Suzuki Y, Kobayashi Y, Daito T, et al. (2010) Endogenous non-retroviral RNA virus elements in mammalian genomes. Nature 463: 84-87.
56. Li Y, Ge X, Zhang H, Zhou P, Zhu Y, et al. (2010) Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol 84: 3889-3897.
57. Sonntag M, Muhldorfer K, Speck S, Wibbelt G, Kurth A (2009) New adenovirus in bats, Germany. Emerg Infect Dis 15: 2052-2055.
58. Cheval J, Sauvage V, Frangeul L, Dacheux L, Guigon G, et al. (2011) Evaluation of high-throughput sequencing for identifying known and unknown viruses in biological samples. J Clin Microbiol 49: 3268-3275.
59. Socolovschi C, Kernif T, Raoult D, Parola P (2012) Borrelia, Rickettsia, and Ehrlichia species in bat ticks, France, 2010. Emerg Infect Dis 18: 1966-1975.
60. Parola P, Raoult D (2001) Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis 32: 897-928. (Pubitemid 32524824)
61. Estes MK, Kang G, Zeng CQ, Crawford SE, Ciarlet M (2001) Pathogenesis of rotavirus gastroenteritis. Novartis Found Symp 238: 82-96; discussion 96-100.
62. Esona MD, Mijatovic-Rustempasic S, Conrardy C, Tong S, Kuzmin IV, et al. (2010) Reassortant group A rotavirus from straw-colored fruit bat (Eidolon helvum). Emerg Infect Dis 16: 1844-1852.
63. Thalmann CM, Cummins DM, Yu M, Lunt R, Pritchard LI, et al. (2010) Broome virus, a new fusogenic Orthoreovirus species isolated from an Australian fruit bat. Virology 402: 26-40.
64. Lelli D, Moreno A, Lavazza A, Bresaola M, Canelli E, et al. (2013) Identification of Mammalian orthoreovirus type 3 in Italian bats. Zoonoses Public Health 60: 84-92.
65. Chua KB, Voon K, Crameri G, Tan HS, Rosli J, et al. (2008) Identification and characterization of a new orthoreovirus from patients with acute respiratory infections. PLoS One 3: e3803.
66. Chua KB, Crameri G, Hyatt A, Yu M, Tompang MR, et al. (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. (Pubitemid 47175156)
67. Brussow H, Nakagomi O, Gerna G, Eichhorn W (1992) Isolation of an avianlike group A rotavirus from a calf with diarrhea. J Clin Microbiol 30: 67-73.
68. Matthijnssens J, Rahman M, Martella V, Xuelei Y, De Vos S, et al. (2006) Full genomic analysis of human rotavirus strain B4106 and lapine rotavirus strain 30/96 provides evidence for interspecies transmission. J Virol 80: 3801-3810.
69. Estes MK, Kapikian AZ (2007) Rotaviruses and their replication. In: Knipe DM, Howley PM, Griffin DE, al e, editors. Fields Virology. 5th Edition ed. PA, USA: Lippincott, Williams and Wilkins. 1917-1974.
70. Parashar UD, Gibson CJ, Bresee JS, Glass RI (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12: 304-306.
71. Fenaux M, Cuadras MA, Feng N, Jaimes M, Greenberg HB (2006) Extraintestinal spread and replication of a homologous EC rotavirus strain and a heterologous rhesus rotavirus in BALB/c mice. J Virol 80: 5219-5232.
72. Crawford SE, Patel DG, Cheng E, Berkova Z, Hyser JM, et al. (2006) Rotavirus viremia and extraintestinal viral infection in the neonatal rat model. J Virol 80: 4820-4832.
73. Kim HJ, Park JG, Matthijnssens J, Lee JH, Bae YC, et al. (2011) Intestinal and extra-intestinal pathogenicity of a bovine reassortant rotavirus in calves and piglets. Vet Microbiol 152: 291-303.
74. Cui J, Tachedjian G, Tachedjian M, Holmes EC, Zhang S, et al. (2012) Identification of diverse groups of endogenous gammaretroviruses in mega- and microbats. J Gen Virol 93: 2037-2045.
75. Cui J, Tachedjian M, Wang L, Tachedjian G, Wang LF, et al. (2012) Discovery of retroviral homologs in bats: implications for the origin of mammalian gammaretroviruses. J Virol 86: 4288-4293.
76. Belyi VA, Levine AJ, Skalka AM (2010) Sequences from ancestral single-stranded DNA viruses in vertebrate genomes: the parvoviridae and circoviridae are more than 40 to 50 million years old. J Virol 84: 12458-12462.
77. Maeda K, Hondo E, Terakawa J, Kiso Y, Nakaichi N, et al. (2008) Isolation of novel adenovirus from fruit bat (Pteropus dasymallus yayeyamae). Emerg Infect Dis 14: 347-349. (Pubitemid 351213699)
78. Ganesh B, Banyai K, Martella V, Jakab F, Masachessi G, et al. (2012) Picobirnavirus infections: viral persistence and zoonotic potential. Rev Med Virol 22: 245-256
79. van Leeuwen M, Williams MM, Koraka P, Simon JH, Smits SL, et al. (2010) Human picobirnaviruses identified by molecular screening of diarrhea samples. J Clin Microbiol 48: 1787-1794.
80. Kapusinszky B, Minor P, Delwart E (2012) Nearly constant shedding of diverse enteric viruses by two healthy infants. J Clin Microbiol 50: 3427-3434.
81. Victoria JG, Kapoor A, Li L, Blinkova O, Slikas B, et al. (2009) Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 83: 4642-4651.
82. Smits SL, van Leeuwen M, Schapendonk CM, Schurch AC, Bodewes R, et al. (2012) Picobirnaviruses in the human respiratory tract. Emerg Infect Dis 18: 1539-1540.
83. Smits SL, Poon LL, van Leeuwen M, Lau PN, Perera HK, et al. (2011) Genogroup I and II picobirnaviruses in respiratory tracts of pigs. Emerg Infect Dis 17: 2328-2330.
84. Giordano MO, Martinez LC, Masachessi G, Barril PA, Ferreyra LJ, et al. (2011) Evidence of closely related picobirnavirus strains circulating in humans and pigs in Argentina. J Infect 62: 45-51.
85. Banyai K, Martella V, Bogdan A, Forgach P, Jakab F, et al. (2008) Genogroup I picobirnaviruses in pigs: evidence for genetic diversity and relatedness to human strains. J Gen Virol 89: 534-539. (Pubitemid 351622451)
86. Marriott AC, Nuttall PA (1996) Large RNA segment of Dugbe nairovirus encodes the putative RNA polymerase. J Gen Virol 77 (Pt 8): 1775-1780. (Pubitemid 26278756)
87. Muller R, Poch O, Delarue M, Bishop DH, Bouloy M (1994) Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J Gen Virol 75 (Pt 6): 1345-1352.