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Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Research

Viral metagenomic analysis of feces of wild small carnivores

Authors: Rogier Bodewes, Aritz Ruiz-Gonzalez, Claudia ME Schapendonk, Judith MA van den Brand, Albert DME Osterhaus, Saskia L Smits

Published in: Virology Journal | Issue 1/2014

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Abstract

Background

Recent studies have clearly demonstrated the enormous virus diversity that exists among wild animals. This exemplifies the required expansion of our knowledge of the virus diversity present in wildlife, as well as the potential transmission of these viruses to domestic animals or humans.

Methods

In the present study we evaluated the viral diversity of fecal samples (n = 42) collected from 10 different species of wild small carnivores inhabiting the northern part of Spain using random PCR in combination with next-generation sequencing. Samples were collected from American mink (Neovison vison), European mink (Mustela lutreola), European polecat (Mustela putorius), European pine marten (Martes martes), stone marten (Martes foina), Eurasian otter (Lutra lutra) and Eurasian badger (Meles meles) of the family of Mustelidae; common genet (Genetta genetta) of the family of Viverridae; red fox (Vulpes vulpes) of the family of Canidae and European wild cat (Felis silvestris) of the family of Felidae.

Results

A number of sequences of possible novel viruses or virus variants were detected, including a theilovirus, phleboviruses, an amdovirus, a kobuvirus and picobirnaviruses.

Conclusions

Using random PCR in combination with next generation sequencing, sequences of various novel viruses or virus variants were detected in fecal samples collected from Spanish carnivores. Detected novel viruses highlight the viral diversity that is present in fecal material of wild carnivores.
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Literature
1.
go back to reference Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA: Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012, 367: 1814-1820. 10.1056/NEJMoa1211721.PubMedCrossRef Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA: Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012, 367: 1814-1820. 10.1056/NEJMoa1211721.PubMedCrossRef
2.
go back to reference Reusken CB, Haagmans BL, Müller MA, Gutierrez C, Godeke GJ, Meyer B, Muth D, Raj VS, Smits-De Vries L, Corman VM, Drexler JF, Smits SL, El Tahir YE, De Sousa R, van Beek J, Nowotny N, van Maanen K, Hidalgo-Hermoso E, Bosch BJ, Rottier P, Osterhaus A, Gortázar-Schmidt C, Drosten C, Koopmans MP: Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect Dis. 2013, 13: 859-866. 10.1016/S1473-3099(13)70164-6.PubMedCrossRef Reusken CB, Haagmans BL, Müller MA, Gutierrez C, Godeke GJ, Meyer B, Muth D, Raj VS, Smits-De Vries L, Corman VM, Drexler JF, Smits SL, El Tahir YE, De Sousa R, van Beek J, Nowotny N, van Maanen K, Hidalgo-Hermoso E, Bosch BJ, Rottier P, Osterhaus A, Gortázar-Schmidt C, Drosten C, Koopmans MP: Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect Dis. 2013, 13: 859-866. 10.1016/S1473-3099(13)70164-6.PubMedCrossRef
3.
go back to reference Ithete NL, Stoffberg S, Corman VM, Cottontail VM, Richards LR, Schoeman MC, Drosten C, Drexler JF, Preiser W: Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg Infect Dis. 2013, 19: 1697-1699. 10.3201/eid1910.130946.PubMedPubMedCentralCrossRef Ithete NL, Stoffberg S, Corman VM, Cottontail VM, Richards LR, Schoeman MC, Drosten C, Drexler JF, Preiser W: Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg Infect Dis. 2013, 19: 1697-1699. 10.3201/eid1910.130946.PubMedPubMedCentralCrossRef
4.
go back to reference Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, et al: Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013, 368: 1888-1897. 10.1056/NEJMoa1304459.PubMedCrossRef Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, Chen J, Jie Z, Qiu H, Xu K, Xu X, Lu H, Zhu W, Gao Z, Xiang N, Shen Y, He Z, Gu Y, Zhang Z, Yang Y, Zhao X, Zhou L, Li X, Zou S, Zhang Y, Li X, Yang L, Guo J, Dong J, Li Q, et al: Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013, 368: 1888-1897. 10.1056/NEJMoa1304459.PubMedCrossRef
5.
go back to reference Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, Bi Y, Wu Y, Li X, Yan J, Liu W, Zhao G, Yang W, Wang Y, Ma J, Shu Y, Lei F, Gao GF: Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet. 2013, 381: 1926-1932. 10.1016/S0140-6736(13)60938-1.PubMedCrossRef Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, Bi Y, Wu Y, Li X, Yan J, Liu W, Zhao G, Yang W, Wang Y, Ma J, Shu Y, Lei F, Gao GF: Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet. 2013, 381: 1926-1932. 10.1016/S0140-6736(13)60938-1.PubMedCrossRef
6.
go back to reference Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P: Prediction and prevention of the next pandemic zoonosis. Lancet. 2012, 380: 1956-1965. 10.1016/S0140-6736(12)61684-5.PubMedPubMedCentralCrossRef Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P: Prediction and prevention of the next pandemic zoonosis. Lancet. 2012, 380: 1956-1965. 10.1016/S0140-6736(12)61684-5.PubMedPubMedCentralCrossRef
7.
go back to reference Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL: The fecal viral flora of wild rodents. PLoS Pathog. 2011, 7: e1002218-10.1371/journal.ppat.1002218.PubMedPubMedCentralCrossRef Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL: The fecal viral flora of wild rodents. PLoS Pathog. 2011, 7: e1002218-10.1371/journal.ppat.1002218.PubMedPubMedCentralCrossRef
8.
go back to reference Ge X, Li Y, Yang X, Zhang H, Zhou P, Zhang Y, Shi Z: Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J Virol. 2012, 86: 4620-4630. 10.1128/JVI.06671-11.PubMedPubMedCentralCrossRef Ge X, Li Y, Yang X, Zhang H, Zhou P, Zhang Y, Shi Z: Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J Virol. 2012, 86: 4620-4630. 10.1128/JVI.06671-11.PubMedPubMedCentralCrossRef
9.
go back to reference van den Brand JM, van Leeuwen M, Schapendonk CM, Simon JH, Haagmans BL, Osterhaus AD, Smits SL: Metagenomic analysis of the viral flora of pine marten and European badger feces. J Virol. 2012, 86: 2360-2365. 10.1128/JVI.06373-11.PubMedPubMedCentralCrossRef van den Brand JM, van Leeuwen M, Schapendonk CM, Simon JH, Haagmans BL, Osterhaus AD, Smits SL: Metagenomic analysis of the viral flora of pine marten and European badger feces. J Virol. 2012, 86: 2360-2365. 10.1128/JVI.06373-11.PubMedPubMedCentralCrossRef
10.
go back to reference Shan T, Li L, Simmonds P, Wang C, Moeser A, Delwart E: The fecal virome of pigs on a high-density farm. J Virol. 2011, 85: 11697-11708. 10.1128/JVI.05217-11.PubMedPubMedCentralCrossRef Shan T, Li L, Simmonds P, Wang C, Moeser A, Delwart E: The fecal virome of pigs on a high-density farm. J Virol. 2011, 85: 11697-11708. 10.1128/JVI.05217-11.PubMedPubMedCentralCrossRef
11.
go back to reference Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM, Solovyov A, Ojeda-Flores R, Arrigo NC, Islam A, Ali Khan S, Hosseini P, Bogich TL, Olival KJ, Sanchez-Leon MD, Karesh WB, Goldstein T, Luby SP, Morse SS, Mazet JA, Daszak P, Lipkin WI: A strategy to estimate unknown viral diversity in mammals. MBio 3. 2013, 4 (5): e00598-13. Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM, Solovyov A, Ojeda-Flores R, Arrigo NC, Islam A, Ali Khan S, Hosseini P, Bogich TL, Olival KJ, Sanchez-Leon MD, Karesh WB, Goldstein T, Luby SP, Morse SS, Mazet JA, Daszak P, Lipkin WI: A strategy to estimate unknown viral diversity in mammals. MBio 3. 2013, 4 (5): e00598-13.
12.
go back to reference De Benedictis P, Gallo T, Iob A, Coassin R, Squecco G, Ferri G, D’Ancona F, Marangon S, Capua I, Mutinelli F: Emergence of fox rabies in north-eastern Italy. Euro Surveill. 2008, 13: 19033-PubMed De Benedictis P, Gallo T, Iob A, Coassin R, Squecco G, Ferri G, D’Ancona F, Marangon S, Capua I, Mutinelli F: Emergence of fox rabies in north-eastern Italy. Euro Surveill. 2008, 13: 19033-PubMed
13.
go back to reference Johnson N, Freuling C, Vos A, Un H, Valtchovski R, Turcitu M, Dumistrescu F, Vuta V, Velic R, Sandrac V, Aylan O, Müller T, Fooks AR: Epidemiology of rabies in Southeast Europe. Dev Biol (Basel). 2008, 131: 189-198. Johnson N, Freuling C, Vos A, Un H, Valtchovski R, Turcitu M, Dumistrescu F, Vuta V, Velic R, Sandrac V, Aylan O, Müller T, Fooks AR: Epidemiology of rabies in Southeast Europe. Dev Biol (Basel). 2008, 131: 189-198.
14.
go back to reference Bodewes R, van der Giessen J, Haagmans BL, Osterhaus AD, Smits SL: Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes. J Virol. 2013, 87: 7758-7764. 10.1128/JVI.00568-13.PubMedPubMedCentralCrossRef Bodewes R, van der Giessen J, Haagmans BL, Osterhaus AD, Smits SL: Identification of multiple novel viruses, including a parvovirus and a hepevirus, in feces of red foxes. J Virol. 2013, 87: 7758-7764. 10.1128/JVI.00568-13.PubMedPubMedCentralCrossRef
15.
go back to reference Xu B, Zhi N, Hu G, Wan Z, Zheng X, Liu X, Wong S, Kajigaya S, Zhao K, Mao Q, Young NS: Hybrid DNA virus in Chinese patients with seronegative hepatitis discovered by deep sequencing. Proc Natl Acad Sci U S A. 2013, 110: 10264-10269. 10.1073/pnas.1303744110.PubMedPubMedCentralCrossRef Xu B, Zhi N, Hu G, Wan Z, Zheng X, Liu X, Wong S, Kajigaya S, Zhao K, Mao Q, Young NS: Hybrid DNA virus in Chinese patients with seronegative hepatitis discovered by deep sequencing. Proc Natl Acad Sci U S A. 2013, 110: 10264-10269. 10.1073/pnas.1303744110.PubMedPubMedCentralCrossRef
16.
go back to reference Smuts H, Kew M, Khan A, Korsman S: Novel hybrid parvovirus-like virus, NIH-CQV/PHV, contaminants in silica column-based nucleic acid extraction kits. J Virol. 2014, 88: 1398-10.1128/JVI.03206-13.PubMedPubMedCentralCrossRef Smuts H, Kew M, Khan A, Korsman S: Novel hybrid parvovirus-like virus, NIH-CQV/PHV, contaminants in silica column-based nucleic acid extraction kits. J Virol. 2014, 88: 1398-10.1128/JVI.03206-13.PubMedPubMedCentralCrossRef
17.
go back to reference Philipps A, Dauber M, Groth M, Schirrmeier H, Platzer M, Krumbholz A, Wutzler P, Zell R: Isolation and molecular characterization of a second serotype of the encephalomyocarditis virus. Vet Microbiol. 2012, 161: 49-57. 10.1016/j.vetmic.2012.07.006.PubMedCrossRef Philipps A, Dauber M, Groth M, Schirrmeier H, Platzer M, Krumbholz A, Wutzler P, Zell R: Isolation and molecular characterization of a second serotype of the encephalomyocarditis virus. Vet Microbiol. 2012, 161: 49-57. 10.1016/j.vetmic.2012.07.006.PubMedCrossRef
18.
go back to reference Yang B, Wang F, Zhang S, Xu G, Wen Y, Li J, Yang Z, Wu H: Complete genome sequence of a mink calicivirus in China. J Virol. 2012, 86: 13835-10.1128/JVI.02582-12.PubMedPubMedCentralCrossRef Yang B, Wang F, Zhang S, Xu G, Wen Y, Li J, Yang Z, Wu H: Complete genome sequence of a mink calicivirus in China. J Virol. 2012, 86: 13835-10.1128/JVI.02582-12.PubMedPubMedCentralCrossRef
19.
go back to reference Manas S, Cena JC, Ruiz-Olmo J, Palazon S, Domingo M, Wolfinbarger JB, Bloom ME: Aleutian mink disease parvovirus in wild riparian carnivores in Spain. J Wildl Dis. 2001, 37: 138-144. 10.7589/0090-3558-37.1.138.PubMedCrossRef Manas S, Cena JC, Ruiz-Olmo J, Palazon S, Domingo M, Wolfinbarger JB, Bloom ME: Aleutian mink disease parvovirus in wild riparian carnivores in Spain. J Wildl Dis. 2001, 37: 138-144. 10.7589/0090-3558-37.1.138.PubMedCrossRef
20.
go back to reference Sanchez-Migallon Guzman D, Carvajal A, Garcia-Marin JF, Ferreras MC, Perez V, Mitchell M, Urra F, Cena JC: Aleutian disease serology, protein electrophoresis, and pathology of the European mink (Mustela lutreola) from Navarra. Spain J Zoo Wildl Med. 2008, 39: 305-313. 10.1638/2006-0033.1.PubMedCrossRef Sanchez-Migallon Guzman D, Carvajal A, Garcia-Marin JF, Ferreras MC, Perez V, Mitchell M, Urra F, Cena JC: Aleutian disease serology, protein electrophoresis, and pathology of the European mink (Mustela lutreola) from Navarra. Spain J Zoo Wildl Med. 2008, 39: 305-313. 10.1638/2006-0033.1.PubMedCrossRef
21.
go back to reference Fournier-Chambrillon C, Aasted B, Perrot A, Pontier D, Sauvage F, Artois M, Cassiede JM, Chauby X, Dal Molin A, Simon C, Fournier P: Antibodies to Aleutian mink disease parvovirus in free-ranging European mink (Mustela lutreola) and other small carnivores from southwestern France. J Wildl Dis. 2004, 40: 394-402. 10.7589/0090-3558-40.3.394.PubMedCrossRef Fournier-Chambrillon C, Aasted B, Perrot A, Pontier D, Sauvage F, Artois M, Cassiede JM, Chauby X, Dal Molin A, Simon C, Fournier P: Antibodies to Aleutian mink disease parvovirus in free-ranging European mink (Mustela lutreola) and other small carnivores from southwestern France. J Wildl Dis. 2004, 40: 394-402. 10.7589/0090-3558-40.3.394.PubMedCrossRef
23.
go back to reference Brahic M, Bureau JF, Michiels T: The genetics of the persistent infection and demyelinating disease caused by Theiler’s virus. Annu Rev Microbiol. 2005, 59: 279-298. 10.1146/annurev.micro.59.030804.121242.PubMedCrossRef Brahic M, Bureau JF, Michiels T: The genetics of the persistent infection and demyelinating disease caused by Theiler’s virus. Annu Rev Microbiol. 2005, 59: 279-298. 10.1146/annurev.micro.59.030804.121242.PubMedCrossRef
24.
go back to reference Casals J: Immunological characterization of Vilyuisk human encephalomyelitis virus. Nature. 1963, 200: 339-341. 10.1038/200339a0.PubMedCrossRef Casals J: Immunological characterization of Vilyuisk human encephalomyelitis virus. Nature. 1963, 200: 339-341. 10.1038/200339a0.PubMedCrossRef
25.
go back to reference Pritchard AE, Strom T, Lipton HL: Nucleotide sequence identifies Vilyuisk virus as a divergent Theiler’s virus. Virology. 1992, 191: 469-472. 10.1016/0042-6822(92)90212-8.PubMedCrossRef Pritchard AE, Strom T, Lipton HL: Nucleotide sequence identifies Vilyuisk virus as a divergent Theiler’s virus. Virology. 1992, 191: 469-472. 10.1016/0042-6822(92)90212-8.PubMedCrossRef
26.
go back to reference Jones MS, Lukashov VV, Ganac RD, Schnurr DP: Discovery of a novel human picornavirus in a stool sample from a pediatric patient presenting with fever of unknown origin. J Clin Microbiol. 2007, 45: 2144-2150. 10.1128/JCM.00174-07.PubMedPubMedCentralCrossRef Jones MS, Lukashov VV, Ganac RD, Schnurr DP: Discovery of a novel human picornavirus in a stool sample from a pediatric patient presenting with fever of unknown origin. J Clin Microbiol. 2007, 45: 2144-2150. 10.1128/JCM.00174-07.PubMedPubMedCentralCrossRef
27.
28.
go back to reference Zoll J, Erkens Hulshof S, Lanke K, Verduyn Lunel F, Melchers WJ, Schoondermark-Van De Ven E, Roivainen M, Galama JM, Van Kuppeveld FJ: Saffold virus, a human Theiler’s-like cardiovirus, is ubiquitous and causes infection early in life. PLoS Pathog. 2009, 5: e1000416-10.1371/journal.ppat.1000416.PubMedPubMedCentralCrossRef Zoll J, Erkens Hulshof S, Lanke K, Verduyn Lunel F, Melchers WJ, Schoondermark-Van De Ven E, Roivainen M, Galama JM, Van Kuppeveld FJ: Saffold virus, a human Theiler’s-like cardiovirus, is ubiquitous and causes infection early in life. PLoS Pathog. 2009, 5: e1000416-10.1371/journal.ppat.1000416.PubMedPubMedCentralCrossRef
29.
go back to reference Liang Z, Kumar AS, Jones MS, Knowles NJ, Lipton HL: Phylogenetic analysis of the species Theilovirus: emerging murine and human pathogens. J Virol. 2008, 82: 11545-11554. 10.1128/JVI.01160-08.PubMedPubMedCentralCrossRef Liang Z, Kumar AS, Jones MS, Knowles NJ, Lipton HL: Phylogenetic analysis of the species Theilovirus: emerging murine and human pathogens. J Virol. 2008, 82: 11545-11554. 10.1128/JVI.01160-08.PubMedPubMedCentralCrossRef
30.
go back to reference Kobasa D, Mulvey M, Lee JS, Scraba DG: Characterization of Mengo virus neutralization epitopes. II. Infection of mice with an attenuated virus. Virology. 1995, 214: 118-127. 10.1006/viro.1995.9948.PubMedCrossRef Kobasa D, Mulvey M, Lee JS, Scraba DG: Characterization of Mengo virus neutralization epitopes. II. Infection of mice with an attenuated virus. Virology. 1995, 214: 118-127. 10.1006/viro.1995.9948.PubMedCrossRef
31.
go back to reference Kong WP, Roos RP: Alternative translation initiation site in the DA strain of Theiler’s murine encephalomyelitis virus. J Virol. 1991, 65: 3395-3399.PubMedPubMedCentral Kong WP, Roos RP: Alternative translation initiation site in the DA strain of Theiler’s murine encephalomyelitis virus. J Virol. 1991, 65: 3395-3399.PubMedPubMedCentral
32.
go back to reference Palacios G, Tesh R, Savji N, da Rosa APT, Guzman H, Bussetti AV, Desai A, Ladner J, Sanchez-Seco M, Lipkin WI: Characterization of the Sandfly fever Naples species complex and description of a new Karimabad species complex (genus Phlebovirus, family Bunyaviridae). J Gen Virol. 2014, 95 (Pt 2): 292-300.PubMedPubMedCentralCrossRef Palacios G, Tesh R, Savji N, da Rosa APT, Guzman H, Bussetti AV, Desai A, Ladner J, Sanchez-Seco M, Lipkin WI: Characterization of the Sandfly fever Naples species complex and description of a new Karimabad species complex (genus Phlebovirus, family Bunyaviridae). J Gen Virol. 2014, 95 (Pt 2): 292-300.PubMedPubMedCentralCrossRef
33.
go back to reference Palacios G, Savji N, Travassos Da Rosa A, Guzman H, Yu X, Desai A, Rosen GE, Hutchison S, Lipkin WI, Tesh R: Characterization of the Uukuniemi virus group (Phlebovirus: Bunyaviridae): evidence for seven distinct species. J Virol. 2013, 87: 3187-3195. 10.1128/JVI.02719-12.PubMedPubMedCentralCrossRef Palacios G, Savji N, Travassos Da Rosa A, Guzman H, Yu X, Desai A, Rosen GE, Hutchison S, Lipkin WI, Tesh R: Characterization of the Uukuniemi virus group (Phlebovirus: Bunyaviridae): evidence for seven distinct species. J Virol. 2013, 87: 3187-3195. 10.1128/JVI.02719-12.PubMedPubMedCentralCrossRef
34.
go back to reference Swei A, Russell BJ, Naccache SN, Kabre B, Veeraraghavan N, Pilgard MA, Johnson BJ, Chiu CY: The genome sequence of Lone Star virus, a highly divergent bunyavirus found in the Amblyomma americanum tick. PLoS One. 2013, 8: e62083-10.1371/journal.pone.0062083.PubMedPubMedCentralCrossRef Swei A, Russell BJ, Naccache SN, Kabre B, Veeraraghavan N, Pilgard MA, Johnson BJ, Chiu CY: The genome sequence of Lone Star virus, a highly divergent bunyavirus found in the Amblyomma americanum tick. PLoS One. 2013, 8: e62083-10.1371/journal.pone.0062083.PubMedPubMedCentralCrossRef
35.
go back to reference Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, Zhang L, Zhang QF, Popov VL, Li C, Qu J, Li Q, Zhang YP, Hai R, Wu W, Wang Q, Zhan FX, Wang XJ, Kan B, Wang SW, Wan KL, Jing HQ, Lu JX, Yin WW, Zhou H, Guan XH, Liu JF, Bi ZQ, Liu GH, Ren J, et al: Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med. 2011, 364: 1523-1532. 10.1056/NEJMoa1010095.PubMedPubMedCentralCrossRef Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, Zhang L, Zhang QF, Popov VL, Li C, Qu J, Li Q, Zhang YP, Hai R, Wu W, Wang Q, Zhan FX, Wang XJ, Kan B, Wang SW, Wan KL, Jing HQ, Lu JX, Yin WW, Zhou H, Guan XH, Liu JF, Bi ZQ, Liu GH, Ren J, et al: Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med. 2011, 364: 1523-1532. 10.1056/NEJMoa1010095.PubMedPubMedCentralCrossRef
36.
go back to reference Zhang YZ, Zhou DJ, Qin XC, Tian JH, Xiong Y, Wang JB, Chen XP, Gao DY, He YW, Jin D, Sun Q, Guo WP, Wang W, Yu B, Li J, Dai YA, Li W, Peng JS, Zhang GB, Zhang S, Chen XM, Wang Y, Li MH, Lu X, Ye C, de Jong MD, Xu J: The ecology, genetic diversity, and phylogeny of Huaiyangshan virus in China. J Virol. 2012, 86: 2864-2868. 10.1128/JVI.06192-11.PubMedPubMedCentralCrossRef Zhang YZ, Zhou DJ, Qin XC, Tian JH, Xiong Y, Wang JB, Chen XP, Gao DY, He YW, Jin D, Sun Q, Guo WP, Wang W, Yu B, Li J, Dai YA, Li W, Peng JS, Zhang GB, Zhang S, Chen XM, Wang Y, Li MH, Lu X, Ye C, de Jong MD, Xu J: The ecology, genetic diversity, and phylogeny of Huaiyangshan virus in China. J Virol. 2012, 86: 2864-2868. 10.1128/JVI.06192-11.PubMedPubMedCentralCrossRef
37.
go back to reference Imam IZ, Darwish MA, El-Karamany R: An epidemic of Rift Valley fever in Egypt. 1. Diagnosis of Rift Valley fever in man. Bull World Health Organ. 1979, 57: 437-439.PubMedPubMedCentral Imam IZ, Darwish MA, El-Karamany R: An epidemic of Rift Valley fever in Egypt. 1. Diagnosis of Rift Valley fever in man. Bull World Health Organ. 1979, 57: 437-439.PubMedPubMedCentral
38.
go back to reference Li L, Pesavento PA, Woods L, Clifford DL, Luff J, Wang C, Delwart E: Novel amdovirus in gray foxes. Emerg Infect Dis. 2011, 17: 1876-1878. 10.3201/eid1710.110233.PubMedPubMedCentralCrossRef Li L, Pesavento PA, Woods L, Clifford DL, Luff J, Wang C, Delwart E: Novel amdovirus in gray foxes. Emerg Infect Dis. 2011, 17: 1876-1878. 10.3201/eid1710.110233.PubMedPubMedCentralCrossRef
39.
go back to reference Yamashita T, Sakae K, Tsuzuki H, Suzuki Y, Ishikawa N, Takeda N, Miyamura T, Yamazaki S: Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. J Virol. 1998, 72: 8408-8412.PubMedPubMedCentral Yamashita T, Sakae K, Tsuzuki H, Suzuki Y, Ishikawa N, Takeda N, Miyamura T, Yamazaki S: Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. J Virol. 1998, 72: 8408-8412.PubMedPubMedCentral
40.
go back to reference Yamashita T, Ito M, Kabashima Y, Tsuzuki H, Fujiura A, Sakae K: Isolation and characterization of a new species of kobuvirus associated with cattle. J Gen Virol. 2003, 84: 3069-3077. 10.1099/vir.0.19266-0.PubMedCrossRef Yamashita T, Ito M, Kabashima Y, Tsuzuki H, Fujiura A, Sakae K: Isolation and characterization of a new species of kobuvirus associated with cattle. J Gen Virol. 2003, 84: 3069-3077. 10.1099/vir.0.19266-0.PubMedCrossRef
41.
go back to reference Reuter G, Boldizsar A, Pankovics P: 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. 2009, 154: 101-108. 10.1007/s00705-008-0288-2.PubMedCrossRef Reuter G, Boldizsar A, Pankovics P: 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. 2009, 154: 101-108. 10.1007/s00705-008-0288-2.PubMedCrossRef
42.
go back to reference Smits SL, Raj VS, Oduber MD, Schapendonk CM, Bodewes R, Provacia L, Stittelaar KJ, Osterhaus AD, Haagmans BL: Metagenomic analysis of the ferret fecal viral flora. PLoS One. 2013, 8: e71595-10.1371/journal.pone.0071595.PubMedPubMedCentralCrossRef Smits SL, Raj VS, Oduber MD, Schapendonk CM, Bodewes R, Provacia L, Stittelaar KJ, Osterhaus AD, Haagmans BL: Metagenomic analysis of the ferret fecal viral flora. PLoS One. 2013, 8: e71595-10.1371/journal.pone.0071595.PubMedPubMedCentralCrossRef
43.
go back to reference Carmona-Vicente N, Buesa J, Brown PA, Merga JY, Darby AC, Stavisky J, Sadler L, Gaskell RM, Dawson S, Radford AD: Phylogeny and prevalence of kobuviruses in dogs and cats in the UK. Vet Microbiol. 2013, 164: 246-252. 10.1016/j.vetmic.2013.02.014.PubMedCrossRef Carmona-Vicente N, Buesa J, Brown PA, Merga JY, Darby AC, Stavisky J, Sadler L, Gaskell RM, Dawson S, Radford AD: Phylogeny and prevalence of kobuviruses in dogs and cats in the UK. Vet Microbiol. 2013, 164: 246-252. 10.1016/j.vetmic.2013.02.014.PubMedCrossRef
44.
go back to reference Ribes JM, Montava R, Tellez-Castillo CJ, Fernandez-Jimenez M, Buesa J: Seroprevalence of Aichi virus in a Spanish population from 2007 to 2008. Clin Vaccine Immunol. 2010, 17: 545-549. 10.1128/CVI.00382-09.PubMedPubMedCentralCrossRef Ribes JM, Montava R, Tellez-Castillo CJ, Fernandez-Jimenez M, Buesa J: Seroprevalence of Aichi virus in a Spanish population from 2007 to 2008. Clin Vaccine Immunol. 2010, 17: 545-549. 10.1128/CVI.00382-09.PubMedPubMedCentralCrossRef
45.
go back to reference Ng TF, Marine R, Wang C, Simmonds P, Kapusinszky B, Bodhidatta L, Oderinde BS, Wommack KE, Delwart E: High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage. J Virol. 2012, 86: 12161-12175. 10.1128/JVI.00869-12.PubMedPubMedCentralCrossRef Ng TF, Marine R, Wang C, Simmonds P, Kapusinszky B, Bodhidatta L, Oderinde BS, Wommack KE, Delwart E: High variety of known and new RNA and DNA viruses of diverse origins in untreated sewage. J Virol. 2012, 86: 12161-12175. 10.1128/JVI.00869-12.PubMedPubMedCentralCrossRef
46.
go back to reference Di Martino B, Di Felice E, Ceci C, Di Profio F, Marsilio F: Canine kobuviruses in diarrhoeic dogs in Italy. Vet Microbiol. 2013, 166: 246-249. 10.1016/j.vetmic.2013.05.007.PubMedCrossRef Di Martino B, Di Felice E, Ceci C, Di Profio F, Marsilio F: Canine kobuviruses in diarrhoeic dogs in Italy. Vet Microbiol. 2013, 166: 246-249. 10.1016/j.vetmic.2013.05.007.PubMedCrossRef
47.
go back to reference Kapoor A, Simmonds P, Dubovi EJ, Qaisar N, Henriquez JA, Medina J, Shields S, Lipkin WI: Characterization of a canine homolog of human Aichivirus. J Virol. 2011, 85: 11520-11525. 10.1128/JVI.05317-11.PubMedPubMedCentralCrossRef Kapoor A, Simmonds P, Dubovi EJ, Qaisar N, Henriquez JA, Medina J, Shields S, Lipkin WI: Characterization of a canine homolog of human Aichivirus. J Virol. 2011, 85: 11520-11525. 10.1128/JVI.05317-11.PubMedPubMedCentralCrossRef
48.
go back to reference Smits SL, van Leeuwen M, Schapendonk CM, Schurch AC, Bodewes R, Haagmans BL, Osterhaus AD: Picobirnaviruses in the human respiratory tract. Emerg Infect Dis. 2012, 18: 1539-1540.PubMedPubMedCentral Smits SL, van Leeuwen M, Schapendonk CM, Schurch AC, Bodewes R, Haagmans BL, Osterhaus AD: Picobirnaviruses in the human respiratory tract. Emerg Infect Dis. 2012, 18: 1539-1540.PubMedPubMedCentral
49.
go back to reference van Leeuwen M, Williams MM, Koraka P, Simon JH, Smits SL, Osterhaus AD: Human picobirnaviruses identified by molecular screening of diarrhea samples. J Clin Microbiol. 2010, 48: 1787-1794. 10.1128/JCM.02452-09.PubMedPubMedCentralCrossRef van Leeuwen M, Williams MM, Koraka P, Simon JH, Smits SL, Osterhaus AD: Human picobirnaviruses identified by molecular screening of diarrhea samples. J Clin Microbiol. 2010, 48: 1787-1794. 10.1128/JCM.02452-09.PubMedPubMedCentralCrossRef
50.
go back to reference Li L, Shan T, Wang C, Cote C, Kolman J, Onions D, Gulland FM, Delwart E: The fecal viral flora of California sea lions. J Virol. 2011, 85: 9909-9917. 10.1128/JVI.05026-11.PubMedPubMedCentralCrossRef Li L, Shan T, Wang C, Cote C, Kolman J, Onions D, Gulland FM, Delwart E: The fecal viral flora of California sea lions. J Virol. 2011, 85: 9909-9917. 10.1128/JVI.05026-11.PubMedPubMedCentralCrossRef
51.
go back to reference Allison AB, Kohler DJ, Fox KA, Brown JD, Gerhold RW, Shearn-Bochsler VI, Dubovi EJ, Parrish CR, Holmes EC: Frequent cross-species transmission of parvoviruses among diverse carnivore hosts. J Virol. 2013, 87: 2342-2347. 10.1128/JVI.02428-12.PubMedPubMedCentralCrossRef Allison AB, Kohler DJ, Fox KA, Brown JD, Gerhold RW, Shearn-Bochsler VI, Dubovi EJ, Parrish CR, Holmes EC: Frequent cross-species transmission of parvoviruses among diverse carnivore hosts. J Virol. 2013, 87: 2342-2347. 10.1128/JVI.02428-12.PubMedPubMedCentralCrossRef
52.
go back to reference Delwart E: Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr Opin Virol. 2012, 2: 344-352. 10.1016/j.coviro.2012.02.012.PubMedPubMedCentralCrossRef Delwart E: Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr Opin Virol. 2012, 2: 344-352. 10.1016/j.coviro.2012.02.012.PubMedPubMedCentralCrossRef
53.
go back to reference Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC: Integrative analysis of environmental sequences using MEGAN4. Genome Res. 2011, 21: 1552-1560. 10.1101/gr.120618.111.PubMedPubMedCentralCrossRef Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC: Integrative analysis of environmental sequences using MEGAN4. Genome Res. 2011, 21: 1552-1560. 10.1101/gr.120618.111.PubMedPubMedCentralCrossRef
54.
go back to reference Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121.PubMedPubMedCentralCrossRef Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121.PubMedPubMedCentralCrossRef
55.
go back to reference Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ: Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009, 25: 1189-1191. 10.1093/bioinformatics/btp033.PubMedPubMedCentralCrossRef Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ: Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009, 25: 1189-1191. 10.1093/bioinformatics/btp033.PubMedPubMedCentralCrossRef
56.
go back to reference Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH: CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 2013, 41: D348-D352. 10.1093/nar/gks1243.PubMedPubMedCentralCrossRef Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH: CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 2013, 41: D348-D352. 10.1093/nar/gks1243.PubMedPubMedCentralCrossRef
Metadata
Title
Viral metagenomic analysis of feces of wild small carnivores
Authors
Rogier Bodewes
Aritz Ruiz-Gonzalez
Claudia ME Schapendonk
Judith MA van den Brand
Albert DME Osterhaus
Saskia L Smits
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-11-89

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