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Published in: Archives of Virology 4/2016

01-04-2016 | Original Article

Metagenomic analysis demonstrates the diversity of the fecal virome in asymptomatic pigs in East Africa

Authors: Joshua O. Amimo, Mohamed E. El Zowalaty, Dedan Githae, Mark Wamalwa, Apollinaire Djikeng, Gheyath K. Nasrallah

Published in: Archives of Virology | Issue 4/2016

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Abstract

Pigs harbor a variety of viruses that are closely related to human viruses and are suspected to have zoonotic potential. Little is known about the presence of viruses in smallholder farms where pigs are in close contact with humans and wildlife. This study provides insight into viral communities and the prevalence and characteristics of enteric viral co-infections in smallholder pigs in East Africa. Sequence-independent amplification and high-throughput sequencing were applied to the metagenomics analysis of viruses in feces collected from asymptomatic pigs. A total of 47,213 de novo-assembled contigs were constructed and compared with sequences from the GenBank database. Blastx search results revealed that 1039 contigs (>200 nt) were related to viral sequences in the GenBank database. Of the 1039 contigs, 612 were not assigned to any viral taxa because they had little similarity to known viral genomic or protein sequences, while 427 contigs had a high level of sequence similarity to known viruses and were assigned to viral taxa. The most frequent contigs related to mammalian viruses resembling members of the viral genera Astrovirus, Rotavirus, Bocavirus, Circovirus, and Kobuvirus. Other less abundant contigs were related to members of the genera Sapelovirus, Pasivirus, Posavirus, Teschovirus and Picobirnavirus. This is the first report on the diversity of the fecal virome of pig populations in East Africa. The findings of the present study help to elucidate the etiology of diarrheal diseases in pigs and identify potential zoonotic and emerging viruses in the region. Further investigations are required to compare the incidence of these viruses in healthy and diseased pigs in order to better elucidate their pathogenic role.
Literature
1.
go back to reference Koopmans M, Duizer E (2004) Foodborne viruses: an emerging problem. Int J Food Microbiol 90(1):23–41CrossRefPubMed Koopmans M, Duizer E (2004) Foodborne viruses: an emerging problem. Int J Food Microbiol 90(1):23–41CrossRefPubMed
2.
go back to reference Dorjee S, Poljak Z, Revie CW, Bridgland J, McNab B, Leger E, Sanchez J (2013) A review of simulation modelling approaches used for the spread of zoonotic influenza viruses in animal and human populations. Zoonoses Public Health 60(6):383–411CrossRefPubMed Dorjee S, Poljak Z, Revie CW, Bridgland J, McNab B, Leger E, Sanchez J (2013) A review of simulation modelling approaches used for the spread of zoonotic influenza viruses in animal and human populations. Zoonoses Public Health 60(6):383–411CrossRefPubMed
3.
go back to reference Milne-Price S, Miazgowicz KL, Munster VJ (2014) The emergence of the Middle East respiratory syndrome coronavirus. Pathog Dis 71(2):121–136CrossRefPubMed Milne-Price S, Miazgowicz KL, Munster VJ (2014) The emergence of the Middle East respiratory syndrome coronavirus. Pathog Dis 71(2):121–136CrossRefPubMed
4.
go back to reference Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JSM, Guan Y, Rambaut A (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459(7250):1122–1125CrossRefPubMed Smith GJD, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JSM, Guan Y, Rambaut A (2009) Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459(7250):1122–1125CrossRefPubMed
5.
go back to reference Song HD, Tu CC, Zhang GW, Wang SY, Zheng K, Lei LC, Chen QX, Gao YW, Zhou HQ, Xiang H, Zheng HJ, Chern SW, Cheng F, Pan CM, Xuan H, Chen SJ, Luo HM, Zhou DH, Liu YF, He JF, Qin PZ, Li LH, Ren YQ, Liang WJ, Yu YD, Anderson L, Wang M, Xu RH, Wu XW, Zheng HY, Chen JD, Liang G, Gao Y, Liao M, Fang L, Jiang LY, Li H, Chen F, Di B, He LJ, Lin JY, Tong S, Kong X, Du L, Hao P, Tang H, Bernini A, Yu XJ, Spiga O, Guo ZM, Pan HY, He WZ, Manuguerra JC, Fontanet A, Danchin A, Niccolai N, Li YX, Wu CI, Zhao GP (2005) Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci USA 102(7):2430–2435CrossRefPubMedPubMedCentral Song HD, Tu CC, Zhang GW, Wang SY, Zheng K, Lei LC, Chen QX, Gao YW, Zhou HQ, Xiang H, Zheng HJ, Chern SW, Cheng F, Pan CM, Xuan H, Chen SJ, Luo HM, Zhou DH, Liu YF, He JF, Qin PZ, Li LH, Ren YQ, Liang WJ, Yu YD, Anderson L, Wang M, Xu RH, Wu XW, Zheng HY, Chen JD, Liang G, Gao Y, Liao M, Fang L, Jiang LY, Li H, Chen F, Di B, He LJ, Lin JY, Tong S, Kong X, Du L, Hao P, Tang H, Bernini A, Yu XJ, Spiga O, Guo ZM, Pan HY, He WZ, Manuguerra JC, Fontanet A, Danchin A, Niccolai N, Li YX, Wu CI, Zhao GP (2005) Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci USA 102(7):2430–2435CrossRefPubMedPubMedCentral
6.
go back to reference Morse SS, Mazet JAK, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P (2012) Prediction and prevention of the next pandemic zoonosis. Lancet 380(9857):1956–1965CrossRefPubMedPubMedCentral Morse SS, Mazet JAK, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P (2012) Prediction and prevention of the next pandemic zoonosis. Lancet 380(9857):1956–1965CrossRefPubMedPubMedCentral
7.
go back to reference Blomstrom AL, Stahl K, Masembe C, Okoth E, Okurut AR, Atmnedi P, Kemp S, Bishop R, Belak S, Berg M (2012) Viral metagenomic analysis of bushpigs (Potamochoerus larvatus) in Uganda identifies novel variants of Porcine parvovirus 4 and Torque teno sus virus 1 and 2. Virol J 9:192CrossRefPubMedPubMedCentral Blomstrom AL, Stahl K, Masembe C, Okoth E, Okurut AR, Atmnedi P, Kemp S, Bishop R, Belak S, Berg M (2012) Viral metagenomic analysis of bushpigs (Potamochoerus larvatus) in Uganda identifies novel variants of Porcine parvovirus 4 and Torque teno sus virus 1 and 2. Virol J 9:192CrossRefPubMedPubMedCentral
8.
go back to reference Masembe C, Michuki G, Onyango M, Rumberia C, Norling M, Bishop RP, Djikeng A, Kemp SJ, Orth A, Skilton RA, Stahl K, Fischer A (2012) Viral metagenomics demonstrates that domestic pigs are a potential reservoir for Ndumu virus. Virol J 9(218):218CrossRefPubMedPubMedCentral Masembe C, Michuki G, Onyango M, Rumberia C, Norling M, Bishop RP, Djikeng A, Kemp SJ, Orth A, Skilton RA, Stahl K, Fischer A (2012) Viral metagenomics demonstrates that domestic pigs are a potential reservoir for Ndumu virus. Virol J 9(218):218CrossRefPubMedPubMedCentral
11.
go back to reference Woo PCY, Lau SKP, Teng JLL, Tsang AKL, Joseph M, Wong EYM, Tang Y, Sivakumar S, Bai R, Wernery R (2014) Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virol 471:117–125CrossRef Woo PCY, Lau SKP, Teng JLL, Tsang AKL, Joseph M, Wong EYM, Tang Y, Sivakumar S, Bai R, Wernery R (2014) Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virol 471:117–125CrossRef
12.
go back to reference J-m Yu, J-s Li, Y-y Ao, Z-j Duan (2013) Detection of novel viruses in porcine fecal samples from China. Virol J 10:39CrossRef J-m Yu, J-s Li, Y-y Ao, Z-j Duan (2013) Detection of novel viruses in porcine fecal samples from China. Virol J 10:39CrossRef
14.
go back to reference Mokili JL, Rohwer F, Dutilh BE (2012) Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2(1):63–77CrossRefPubMed Mokili JL, Rohwer F, Dutilh BE (2012) Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2(1):63–77CrossRefPubMed
15.
go back to reference Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer F (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99(22):14250–14255CrossRefPubMedPubMedCentral Breitbart M, Salamon P, Andresen B, Mahaffy JM, Segall AM, Mead D, Azam F, Rohwer F (2002) Genomic analysis of uncultured marine viral communities. Proc Natl Acad Sci USA 99(22):14250–14255CrossRefPubMedPubMedCentral
17.
go back to reference Smits SL, Raj VS, Oduber MD, Schapendonk CM, Bodewes R, Provacia L, Stittelaar KJ, Osterhaus AD, Haagmans BL (2013) Metagenomic analysis of the ferret fecal viral flora. PLoS One 8(8):e71595CrossRefPubMedPubMedCentral Smits SL, Raj VS, Oduber MD, Schapendonk CM, Bodewes R, Provacia L, Stittelaar KJ, Osterhaus AD, Haagmans BL (2013) Metagenomic analysis of the ferret fecal viral flora. PLoS One 8(8):e71595CrossRefPubMedPubMedCentral
18.
go back to reference Victoria JG, Kapoor A, Li L, Blinkova O, Slikas B, Wang C, Naeem A, Zaidi S, Delwart E (2009) Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 83(9):4642–4651CrossRefPubMedPubMedCentral Victoria JG, Kapoor A, Li L, Blinkova O, Slikas B, Wang C, Naeem A, Zaidi S, Delwart E (2009) Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 83(9):4642–4651CrossRefPubMedPubMedCentral
19.
go back to reference Li L, Shan T, Wang C, Cote C, Kolman J, Onions D, Gulland FM, Delwart E (2011) The fecal viral flora of California sea lions. J Virol 85(19):9909–9917CrossRefPubMedPubMedCentral Li L, Shan T, Wang C, Cote C, Kolman J, Onions D, Gulland FM, Delwart E (2011) The fecal viral flora of California sea lions. J Virol 85(19):9909–9917CrossRefPubMedPubMedCentral
20.
go back to reference Blomstrom AL, Belak S, Fossum C, McKillen J, Allan G, Wallgren P, Berg M (2009) Detection of a novel porcine boca-like virus in the background of porcine circovirus type 2 induced postweaning multisystemic wasting syndrome. Virus Res 146(1–2):125–129CrossRefPubMed Blomstrom AL, Belak S, Fossum C, McKillen J, Allan G, Wallgren P, Berg M (2009) Detection of a novel porcine boca-like virus in the background of porcine circovirus type 2 induced postweaning multisystemic wasting syndrome. Virus Res 146(1–2):125–129CrossRefPubMed
21.
go back to reference Brink M, Stahl K, Masembe C, Okurut AR, Berg M, Blomstrom AL (2012) First time molecular detection and phylogenetic relationships of torque teno sus virus 1 and 2 in domestic pigs in Uganda: further evidence for a global distribution. Virol J 9:39CrossRefPubMedPubMedCentral Brink M, Stahl K, Masembe C, Okurut AR, Berg M, Blomstrom AL (2012) First time molecular detection and phylogenetic relationships of torque teno sus virus 1 and 2 in domestic pigs in Uganda: further evidence for a global distribution. Virol J 9:39CrossRefPubMedPubMedCentral
22.
go back to reference Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512CrossRefPubMed Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512CrossRefPubMed
23.
go back to reference Roux S, Tournayre J, Mahul A, Debroas D, Enault F (2014) Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinform 15(1):76CrossRef Roux S, Tournayre J, Mahul A, Debroas D, Enault F (2014) Metavir 2: new tools for viral metagenome comparison and assembled virome analysis. BMC Bioinform 15(1):76CrossRef
24.
go back to reference Li L, Victoria JG, Wang C, Jones M, Fellers GM, Kunz TH, Delwart E (2010) Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84(14):6955–6965CrossRefPubMedPubMedCentral Li L, Victoria JG, Wang C, Jones M, Fellers GM, Kunz TH, Delwart E (2010) Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84(14):6955–6965CrossRefPubMedPubMedCentral
25.
go back to reference Zhang Q, Hu R, Tang X, Wu C, He Q, Zhao Z, Chen H, Wu B (2013) Occurrence and investigation of enteric viral infections in pigs with diarrhea in China. Arch Virol 158(8):1631–1636CrossRefPubMed Zhang Q, Hu R, Tang X, Wu C, He Q, Zhao Z, Chen H, Wu B (2013) Occurrence and investigation of enteric viral infections in pigs with diarrhea in China. Arch Virol 158(8):1631–1636CrossRefPubMed
26.
27.
go back to reference Quan P-L, Wagner TA, Briese T, Torgerson TR, Hornig M, Tashmukhamedova A, Firth C, Palacios GF, Baisre-de Leon A, Paddock CD (2010) Astrovirus encephalitis in boy with X-linked agammaglobulinemia. Emerg Infect Dis 17(6):918–925CrossRef Quan P-L, Wagner TA, Briese T, Torgerson TR, Hornig M, Tashmukhamedova A, Firth C, Palacios GF, Baisre-de Leon A, Paddock CD (2010) Astrovirus encephalitis in boy with X-linked agammaglobulinemia. Emerg Infect Dis 17(6):918–925CrossRef
28.
go back to reference Rivera R, Nollens HH, Venn-Watson S, Gulland FM, Wellehan JF Jr (2010) Characterization of phylogenetically diverse astroviruses of marine mammals. J Gen Virol 91(Pt 1):166–173CrossRefPubMed Rivera R, Nollens HH, Venn-Watson S, Gulland FM, Wellehan JF Jr (2010) Characterization of phylogenetically diverse astroviruses of marine mammals. J Gen Virol 91(Pt 1):166–173CrossRefPubMed
29.
go back to reference Toffan A, Jonassen CM, De Battisti C, Schiavon E, Kofstad T, Capua I, Cattoli G (2009) Genetic characterization of a new astrovirus detected in dogs suffering from diarrhoea. Vet Microbiol 139(1–2):147–152CrossRefPubMed Toffan A, Jonassen CM, De Battisti C, Schiavon E, Kofstad T, Capua I, Cattoli G (2009) Genetic characterization of a new astrovirus detected in dogs suffering from diarrhoea. Vet Microbiol 139(1–2):147–152CrossRefPubMed
30.
go back to reference Zhu HC, Chu DK, Liu W, Dong BQ, Zhang SY, Zhang JX, Li LF, Vijaykrishna D, Smith GJ, Chen HL, Poon LL, Peiris JS, Guan Y (2009) Detection of diverse astroviruses from bats in China. J Gen Virol 90(Pt 4):883–887CrossRefPubMed Zhu HC, Chu DK, Liu W, Dong BQ, Zhang SY, Zhang JX, Li LF, Vijaykrishna D, Smith GJ, Chen HL, Poon LL, Peiris JS, Guan Y (2009) Detection of diverse astroviruses from bats in China. J Gen Virol 90(Pt 4):883–887CrossRefPubMed
31.
go back to reference Amimo JO, Okoth E, Junga JO, Ogara WO, Njahira MN, Wang Q, Vlasova AN, Saif LJ, Djikeng A (2014) Molecular detection and genetic characterization of kobuviruses and astroviruses in asymptomatic local pigs in East Africa. Arch Virol 159(6):1313–1319CrossRefPubMedPubMedCentral Amimo JO, Okoth E, Junga JO, Ogara WO, Njahira MN, Wang Q, Vlasova AN, Saif LJ, Djikeng A (2014) Molecular detection and genetic characterization of kobuviruses and astroviruses in asymptomatic local pigs in East Africa. Arch Virol 159(6):1313–1319CrossRefPubMedPubMedCentral
32.
go back to reference Luo Z, Roi S, Dastor M, Gallice E, Laurin M-A, L’homme Y (2010) Multiple novel and prevalent astroviruses in pigs. Vet Microbiol 149:316–323CrossRefPubMed Luo Z, Roi S, Dastor M, Gallice E, Laurin M-A, L’homme Y (2010) Multiple novel and prevalent astroviruses in pigs. Vet Microbiol 149:316–323CrossRefPubMed
33.
go back to reference Allander T, Tammi MT, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B (2005) Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci USA 102(36):12891–12896CrossRefPubMedPubMedCentral Allander T, Tammi MT, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B (2005) Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci USA 102(36):12891–12896CrossRefPubMedPubMedCentral
34.
35.
go back to reference W-x Cheng, J-s Li, C-p Huang, D-p Yao, Liu N, S-x Cui, Jin Y, Z-j Duan (2010) Identification and nearly full-length genome characterization of novel porcine bocaviruses. PLoS One 5(10):e13583CrossRef W-x Cheng, J-s Li, C-p Huang, D-p Yao, Liu N, S-x Cui, Jin Y, Z-j Duan (2010) Identification and nearly full-length genome characterization of novel porcine bocaviruses. PLoS One 5(10):e13583CrossRef
36.
go back to reference Zeng S, Wang D, Fang L, Ma J, Song T, Zhang R, Chen H, Xiao S (2011) Complete coding sequences and phylogenetic analysis of porcine bocavirus. J Gen Virol 92(4):784–788CrossRefPubMed Zeng S, Wang D, Fang L, Ma J, Song T, Zhang R, Chen H, Xiao S (2011) Complete coding sequences and phylogenetic analysis of porcine bocavirus. J Gen Virol 92(4):784–788CrossRefPubMed
38.
go back to reference Xiao CT, Halbur PG, Opriessnig T (2013) Molecular evolutionary genetic analysis of emerging parvoviruses identified in pigs. Infect Genet Evol 16:369–376CrossRefPubMed Xiao CT, Halbur PG, Opriessnig T (2013) Molecular evolutionary genetic analysis of emerging parvoviruses identified in pigs. Infect Genet Evol 16:369–376CrossRefPubMed
39.
go back to reference Kapoor A, Simmonds P, Slikas E, Li L, Bodhidatta L, Sethabutr O, Triki H, Bahri O, Oderinde BS, Baba MM, Bukbuk DN, Besser J, Bartkus J, Delwart E (2010) Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J Infect Dis 201(11):1633–1643CrossRefPubMedPubMedCentral Kapoor A, Simmonds P, Slikas E, Li L, Bodhidatta L, Sethabutr O, Triki H, Bahri O, Oderinde BS, Baba MM, Bukbuk DN, Besser J, Bartkus J, Delwart E (2010) Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J Infect Dis 201(11):1633–1643CrossRefPubMedPubMedCentral
40.
go back to reference Amimo JO, Junga JO, Ogara WO, Vlasova AN, Njahira MN, Maina S, Okoth EA, Bishop RP, Saif LJ, Djikeng A (2015) Detection and genetic characterization of porcine group A rotaviruses in asymptomatic pigs in smallholder farms in East Africa: predominance of P[8] genotype resembling human strains. Vet Microbiol 175(2–4):195–210CrossRefPubMed Amimo JO, Junga JO, Ogara WO, Vlasova AN, Njahira MN, Maina S, Okoth EA, Bishop RP, Saif LJ, Djikeng A (2015) Detection and genetic characterization of porcine group A rotaviruses in asymptomatic pigs in smallholder farms in East Africa: predominance of P[8] genotype resembling human strains. Vet Microbiol 175(2–4):195–210CrossRefPubMed
41.
go back to reference Pereira HG, Fialho AM, Flewett TH, Teixeira JMS, Andrade ZP (1988) Novel viruses in human faeces. Lancet 332(8602):103–104CrossRef Pereira HG, Fialho AM, Flewett TH, Teixeira JMS, Andrade ZP (1988) Novel viruses in human faeces. Lancet 332(8602):103–104CrossRef
42.
go back to reference Pereira HG, Flewett TH, Candeias JAN, Barth OM (1988) A virus with a bisegmented double-stranded RNA genome in rat. J Gen Virol 69:2749–2754CrossRefPubMed Pereira HG, Flewett TH, Candeias JAN, Barth OM (1988) A virus with a bisegmented double-stranded RNA genome in rat. J Gen Virol 69:2749–2754CrossRefPubMed
43.
go back to reference Masachessi G, Martínez LC, Giordano MO, Barril PA, Isa BM, Ferreyra L, Villareal D, Carello M, Asis C, Nates SV (2007) Picobirnavirus (PBV) natural hosts in captivity and virus excretion pattern in infected animals. Arch Virol 152(5):989–998CrossRefPubMed Masachessi G, Martínez LC, Giordano MO, Barril PA, Isa BM, Ferreyra L, Villareal D, Carello M, Asis C, Nates SV (2007) Picobirnavirus (PBV) natural hosts in captivity and virus excretion pattern in infected animals. Arch Virol 152(5):989–998CrossRefPubMed
44.
go back to reference Nates SV, Gatti MSV, Ludert JE (2011) The picobirnavirus: an integrated view on its biology, epidemiology and pathogenic potential. Future Virol 6(2):223–235CrossRef Nates SV, Gatti MSV, Ludert JE (2011) The picobirnavirus: an integrated view on its biology, epidemiology and pathogenic potential. Future Virol 6(2):223–235CrossRef
45.
go back to reference King AMQ, Adams MJ, Lefkowitz EJ (2011) Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses, vol 9. Elsevier, Amsterdam King AMQ, Adams MJ, Lefkowitz EJ (2011) Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses, vol 9. Elsevier, Amsterdam
46.
go back to reference Banyai K, Martella V, Bogdan A, Forgach P, Jakab F, Meleg E, Biro H, Melegh B, Szucs G (2008) Genogroup I picobirnaviruses in pigs: evidence for genetic diversity and relatedness to human strains. J Gen Virol 89(2):534–539CrossRefPubMed Banyai K, Martella V, Bogdan A, Forgach P, Jakab F, Meleg E, Biro H, Melegh B, Szucs G (2008) Genogroup I picobirnaviruses in pigs: evidence for genetic diversity and relatedness to human strains. J Gen Virol 89(2):534–539CrossRefPubMed
47.
go back to reference Chen M, Sun H, Lan D, Hua X, Cui L, Yuan C, Yang Z (2014) Molecular detection of genogroup I and II picobirnaviruses in pigs in China. Virus Genes 48(3):553–556CrossRefPubMed Chen M, Sun H, Lan D, Hua X, Cui L, Yuan C, Yang Z (2014) Molecular detection of genogroup I and II picobirnaviruses in pigs in China. Virus Genes 48(3):553–556CrossRefPubMed
48.
go back to reference Smits SL, Poon LL, van Leeuwen M, Lau P-N, Perera HK, Peiris JS, Simon JH, Osterhaus AD (2011) Genogroup I and II picobirnaviruses in respiratory tracts of pigs. Emerg Infect Dis 17(12):2328–2330CrossRefPubMedPubMedCentral Smits SL, Poon LL, van Leeuwen M, Lau P-N, Perera HK, Peiris JS, Simon JH, Osterhaus AD (2011) Genogroup I and II picobirnaviruses in respiratory tracts of pigs. Emerg Infect Dis 17(12):2328–2330CrossRefPubMedPubMedCentral
49.
go back to reference Cheung AK, Ng TF, Lager KM, Bayles DO, Alt DP, Delwart EL, Pogranichniy RM, Kehrli ME Jr (2013) A divergent clade of circular single-stranded DNA viruses from pig feces. Arch Virol 158(10):2157–2162CrossRefPubMedPubMedCentral Cheung AK, Ng TF, Lager KM, Bayles DO, Alt DP, Delwart EL, Pogranichniy RM, Kehrli ME Jr (2013) A divergent clade of circular single-stranded DNA viruses from pig feces. Arch Virol 158(10):2157–2162CrossRefPubMedPubMedCentral
50.
go back to reference Sachsenröder J, Twardziok SO, Scheuch M, Johne R (2014) The general composition of the faecal virome of pigs depends on age, but not on feeding with a probiotic bacterium. PLoS One 9:e88888CrossRefPubMedPubMedCentral Sachsenröder J, Twardziok SO, Scheuch M, Johne R (2014) The general composition of the faecal virome of pigs depends on age, but not on feeding with a probiotic bacterium. PLoS One 9:e88888CrossRefPubMedPubMedCentral
51.
go back to reference Knowles E, Delwart E, Gorbalenya AE, Hovi T, Hyypia T, King AMQ, LinBerg AM, Pallansch MA, Palmenberg AC, Reuter Gb (2014) Picornaviridae: 26 genera, 46 species and growing. In: EUROPIC 2014: XVIII meeting of the European Study Group on the Molecular Biology of Picornaviruses, Blankenberge, pp 9–14 Knowles E, Delwart E, Gorbalenya AE, Hovi T, Hyypia T, King AMQ, LinBerg AM, Pallansch MA, Palmenberg AC, Reuter Gb (2014) Picornaviridae: 26 genera, 46 species and growing. In: EUROPIC 2014: XVIII meeting of the European Study Group on the Molecular Biology of Picornaviruses, Blankenberge, pp 9–14
53.
54.
55.
go back to reference Sisay Z, Wang Q, Oka T, Saif L (2013) Prevalence and molecular characterization of porcine enteric caliciviruses and first detection of porcine kobuviruses in US swine. Arch Virol 158:1583–1588CrossRefPubMedPubMedCentral Sisay Z, Wang Q, Oka T, Saif L (2013) Prevalence and molecular characterization of porcine enteric caliciviruses and first detection of porcine kobuviruses in US swine. Arch Virol 158:1583–1588CrossRefPubMedPubMedCentral
56.
go back to reference Okitsu S, Khamrin P, Thongprachum A, Hidaka S, Kongkaew S, Kongkaew A, Maneekarn N, Mizuguchi M, Hayakawa S, Ushijima H (2012) Sequence analysis of porcine kobuvirus VP1 region detected in pigs in Japan and Thailand. Virus Genes 44:253–257CrossRefPubMed Okitsu S, Khamrin P, Thongprachum A, Hidaka S, Kongkaew S, Kongkaew A, Maneekarn N, Mizuguchi M, Hayakawa S, Ushijima H (2012) Sequence analysis of porcine kobuvirus VP1 region detected in pigs in Japan and Thailand. Virus Genes 44:253–257CrossRefPubMed
57.
go back to reference Haugegaard J (2010) Prevalence of nematodes in Danish industrialized sow farms with loose housed sows in dynamic groups. Vet Parasitol 168(1):156–159CrossRefPubMed Haugegaard J (2010) Prevalence of nematodes in Danish industrialized sow farms with loose housed sows in dynamic groups. Vet Parasitol 168(1):156–159CrossRefPubMed
58.
go back to reference Sauvage V, Gouilh MA, Cheval J, Muth E, Pariente K, Burguiere A, Vr Caro, Manuguerra J-C, Eloit M (2012) A member of a new picornaviridae genus is shed in pig feces. J Virol 86(18):10036–10046CrossRefPubMedPubMedCentral Sauvage V, Gouilh MA, Cheval J, Muth E, Pariente K, Burguiere A, Vr Caro, Manuguerra J-C, Eloit M (2012) A member of a new picornaviridae genus is shed in pig feces. J Virol 86(18):10036–10046CrossRefPubMedPubMedCentral
59.
go back to reference Lan D, Ji W, Yang S, Cui L, Yang Z, Yuan C, Hua X (2011) Isolation and characterization of the first Chinese porcine sapelovirus strain. Arch Virol 156(9):1567–1574CrossRefPubMed Lan D, Ji W, Yang S, Cui L, Yang Z, Yuan C, Hua X (2011) Isolation and characterization of the first Chinese porcine sapelovirus strain. Arch Virol 156(9):1567–1574CrossRefPubMed
Metadata
Title
Metagenomic analysis demonstrates the diversity of the fecal virome in asymptomatic pigs in East Africa
Authors
Joshua O. Amimo
Mohamed E. El Zowalaty
Dedan Githae
Mark Wamalwa
Apollinaire Djikeng
Gheyath K. Nasrallah
Publication date
01-04-2016
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 4/2016
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-016-2819-6

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