1887

Abstract

Rats are known as reservoirs and vectors for several zoonotic pathogens. However, information on the viruses shed by urban wild rats that could pose a zoonotic risk to human health is scare. Here, intestinal contents from 20 wild Norway rats () collected in the city of Berlin, Germany, were subjected to metagenomic analysis of viral nucleic acids. The determined faecal viromes of rats consisted of a variety of known and unknown viruses, and were highly variable among the individuals. Members of the families and represented the most abundant species. Novel picornaviruses, bocaviruses, sapoviruses and stool-associated circular ssDNA viruses were identified, which showed only low sequence identity to known representatives of the corresponding taxa. In addition, noroviruses and rotaviruses were detected as potential zoonotic gastroenteritis viruses. However, partial-genome sequence analyses indicated that the norovirus was closely related to the recently identified rat norovirus and the rotavirus B was closely related to the rat rotavirus strain IDIR; both viruses clustered separately from respective human virus strains in phylogenetic trees. In contrast, the rotavirus A sequences showed high identity to human and animal strains. Analysis of the nearly complete genome of this virus revealed the known genotypes G3, P[3] and N2 for three of the genome segments, whereas the remaining eight genome segments represented the novel genotypes I20–R11–C11–M10–A22–T14–E18–H13. Our results indicated a high heterogeneity of enteric viruses present in urban wild rats; their ability to be transmitted to humans remains to be assessed in the future.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.070029-0
2014-12-01
2024-11-09
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/12/2734.html?itemId=/content/journal/jgv/10.1099/vir.0.070029-0&mimeType=html&fmt=ahah

References

  1. Afrad M. H., Matthijnssens J., Moni S., Kabir F., Ashrafi A., Rahman M. Z., Faruque A. S., Azim T., Rahman M. 2013; Genetic characterization of a rare bovine-like human VP4 mono-reassortant G6P[8] rotavirus strain detected from an infant in Bangladesh. Infect Genet Evol 19:120–126 [View Article][PubMed]
    [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  4. Amori G., Cristaldi M. 1999; Rattus norvegicus. In The Atlas of European Mammals pp. 278–279 Edited by Mitchell-Jones A. J., Amori G., Bogdanowicz W., Kryštufek B., Reijnder P. J. H., Spitzenberger F., Stubbe M., Thissen J. B. M., Vohraík V., Zima J. London: T. & A. D. Poyser;
    [Google Scholar]
  5. Baker D. G. 1998; Natural pathogens of laboratory mice, rats, and rabbits and their effects on research. Clin Microbiol Rev 11:231–266[PubMed]
    [Google Scholar]
  6. Belák S., Karlsson O. E., Blomström A. L., Berg M., Granberg F. 2013; New viruses in veterinary medicine, detected by metagenomic approaches. Vet Microbiol 165:95–101 [View Article][PubMed]
    [Google Scholar]
  7. Blinkova O., Kapoor A., Victoria J., Jones M., Wolfe N., Naeem A., Shaukat S., Sharif S., Alam M. M.other authors 2009; Cardioviruses are genetically diverse and cause common enteric infections in South Asian children. J Virol 83:4631–4641 [View Article][PubMed]
    [Google Scholar]
  8. Blinkova O., Victoria J., Li Y., Keele B. F., Sanz C., Ndjango J. B., Peeters M., Travis D., Lonsdorf E. V.other authors 2010; Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 91:74–86 [View Article][PubMed]
    [Google Scholar]
  9. Breitbart M., Rohwer F. 2005; Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing. Biotechniques 39:729–736 [View Article][PubMed]
    [Google Scholar]
  10. Brugere-Picoux J., Tessier P. 2010; [Viral gastroenteritis in domestic animals and zoonoses]. Bull Acad Natl Med 194:1439–1449 (in French) [PubMed]
    [Google Scholar]
  11. Cahais V., Gayral P., Tsagkogeorga G., Melo-Ferreira J., Ballenghien M., Weinert L., Chiari Y., Belkhir K., Ranwez V., Galtier N. 2012; Reference-free transcriptome assembly in non-model animals from next-generation sequencing data. Mol Ecol Resour 12:834–845 [View Article][PubMed]
    [Google Scholar]
  12. Chow B. D., Esper F. P. 2009; The human bocaviruses: a review and discussion of their role in infection. Clin Lab Med 29:695–713 [View Article][PubMed]
    [Google Scholar]
  13. Cotmore S. F., Agbandje-McKenna M., Chiorini J. A., Mukha D. V., Pintel D. J., Qiu J., Soderlund-Venermo M., Tattersall P., Tijssen P.other authors 2014; The family Parvoviridae.. Arch Virol 159:1239–1247 [View Article][PubMed]
    [Google Scholar]
  14. Doi K. 2011; Experimental encephalomyocarditis virus infection in small laboratory rodents. J Comp Pathol 144:25–40 [View Article][PubMed]
    [Google Scholar]
  15. Dremsek P., Wenzel J. J., Johne R., Ziller M., Hofmann J., Groschup M. H., Werdermann S., Mohn U., Dorn S.other authors 2012; Seroprevalence study in forestry workers from eastern Germany using novel genotype 3- and rat hepatitis E virus-specific immunoglobulin G ELISAs. Med Microbiol Immunol (Berl) 201:189–200 [View Article][PubMed]
    [Google Scholar]
  16. Eckardt A. J., Baumgart D. C. 2011; Viral gastroenteritis in adults. Recent Pat Antiinfect Drug Discov 6:54–63 [View Article][PubMed]
    [Google Scholar]
  17. Ehlers B., Küchler J., Yasmum N., Dural G., Voigt S., Schmidt-Chanasit J., Jäkel T., Matuschka F. R., Richter D.other authors 2007; Identification of novel rodent herpesviruses, including the first gammaherpesvirus of Mus musculus. J Virol 81:8091–8100 [View Article][PubMed]
    [Google Scholar]
  18. Fregolente M. C., de Castro-Dias E., Martins S. S., Spilki F. R., Allegretti S. M., Gatti M. S. 2009; Molecular characterization of picobirnaviruses from new hosts. Virus Res 143:134–136 [View Article][PubMed]
    [Google Scholar]
  19. Guenther S., Bethe A., Fruth A., Semmler T., Ulrich R. G., Wieler L. H., Ewers C. 2012; Frequent combination of antimicrobial multiresistance and extraintestinal pathogenicity in Escherichia coli isolates from urban rats (Rattus norvegicus) in Berlin, Germany. PLoS ONE 7:e50331 [View Article][PubMed]
    [Google Scholar]
  20. Hansman G. S., Oka T., Katayama K., Takeda N. 2007; Human sapoviruses: genetic diversity, recombination, and classification. Rev Med Virol 17:133–141 [View Article][PubMed]
    [Google Scholar]
  21. He B., Yang F., Yang W., Zhang Y., Feng Y., Zhou J., Xie J., Feng Y., Bao X.other authors 2013; Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J Virol 87:12357–12366 [View Article][PubMed]
    [Google Scholar]
  22. Himsworth C. G., Parsons K. L., Jardine C., Patrick D. M. 2013; Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector Borne Zoonotic Dis 13:349–359 [View Article][PubMed]
    [Google Scholar]
  23. Huber A. C., Yolken R. H., Mader L. C., Strandberg J. D., Vonderfecht S. L. 1989; Pathology of infectious diarrhea of infant rats (IDIR) induced by an antigenically distinct rotavirus. Vet Pathol 26:376–385[PubMed]
    [Google Scholar]
  24. Jacoby R. O., Ball-Goodrich L. J., Besselsen D. G., McKisic M. D., Riley L. K., Smith A. L. 1996; Rodent parvovirus infections. Lab Anim Sci 46:370–380[PubMed]
    [Google Scholar]
  25. Ji Y., Shi Y., Ding G., Li Y. 2011; A new strategy for better genome assembly from very short reads. BMC Bioinformatics 12:493 [View Article][PubMed]
    [Google Scholar]
  26. Johne R., Müller H., Rector A., van Ranst M., Stevens H. 2009; Rolling-circle amplification of viral DNA genomes using phi29 polymerase. Trends Microbiol 17:205–211 [View Article][PubMed]
    [Google Scholar]
  27. Johne R., Heckel G., Plenge-Bönig A., Kindler E., Maresch C., Reetz J., Schielke A., Ulrich R. G. 2010; Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis 16:1452–1455 [View Article][PubMed]
    [Google Scholar]
  28. Johne R., Dremsek P., Kindler E., Schielke A., Plenge-Bönig A., Gregersen H., Wessels U., Schmidt K., Rietschel W.other authors 2012; Rat hepatitis E virus: geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). Infect Genet Evol 12:947–956 [View Article][PubMed]
    [Google Scholar]
  29. Jørgensen T. S., Xu Z., Hansen M. A., Sørensen S. J., Hansen L. H. 2014; Hundreds of circular novel plasmids and DNA elements identified in a rat cecum metamobilome. PLoS ONE 9:e87924 [View Article][PubMed]
    [Google Scholar]
  30. Kamar N., Dalton H. R., Abravanel F., Izopet J. 2014; Hepatitis E virus infection. Clin Microbiol Rev 27:116–138 [View Article][PubMed]
    [Google Scholar]
  31. Lee R. M., Lessler J., Lee R. A., Rudolph K. E., Reich N. G., Perl T. M., Cummings D. A. 2013; Incubation periods of viral gastroenteritis: a systematic review. BMC Infect Dis 13:446 [View Article][PubMed]
    [Google Scholar]
  32. Machnowska P., Ellerbroek L., Johne R. 2014; Detection and characterization of potentially zoonotic viruses in faeces of pigs at slaughter in Germany. Vet Microbiol 168:60–68 [View Article][PubMed]
    [Google Scholar]
  33. Manteufel J., Truyen U. 2008; Animal bocaviruses: a brief review. Intervirology 51:328–334 [View Article][PubMed]
    [Google Scholar]
  34. Martella V., Bányai K., Matthijnssens J., Buonavoglia C., Ciarlet M. 2010; Zoonotic aspects of rotaviruses. Vet Microbiol 140:246–255 [View Article][PubMed]
    [Google Scholar]
  35. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Banyai K., Estes M. K., Gentsch J. R., Iturriza-Gomara M., Kirkwood C. D.other authors 2008; Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 153:1621–1629 [View Article][PubMed]
    [Google Scholar]
  36. Matthijnssens J., Ciarlet M., McDonald S. M., Attoui H., Bányai K., Brister J. R., Buesa J., Esona M. D., Estes M. K.other authors 2011; Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156:1397–1413 [View Article][PubMed]
    [Google Scholar]
  37. Meerburg B. G., Singleton G. R., Kijlstra A. 2009; Rodent-borne diseases and their risks for public health. Crit Rev Microbiol 35:221–270 [View Article][PubMed]
    [Google Scholar]
  38. Musser G. G., Carleton M. D. 2005; Rodentia: Myomorpha: Muroidea: Muridae: Murinae. In Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd edn. vol. 1 pp. 1478–1480 Edited by Wilson D. E., Reeder D. M. Baltimore, MD: The Johns Hopkins University Press;
    [Google Scholar]
  39. 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 [View Article][PubMed]
    [Google Scholar]
  40. Pang X. L., Lee B., Boroumand N., Leblanc B., Preiksaitis J. K., Yu Ip C. C. 2004; Increased detection of rotavirus using a real time reverse transcription-polymerase chain reaction (RT-PCR) assay in stool specimens from children with diarrhea. J Med Virol 72:496–501 [View Article][PubMed]
    [Google Scholar]
  41. 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 [View Article][PubMed]
    [Google Scholar]
  42. 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 [View Article][PubMed]
    [Google Scholar]
  43. 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 [View Article][PubMed]
    [Google Scholar]
  44. Rosario K., Duffy S., Breitbart M. 2009; Diverse circovirus-like genome architectures revealed by environmental metagenomics. J Gen Virol 90:2418–2424 [View Article][PubMed]
    [Google Scholar]
  45. 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 [View Article][PubMed]
    [Google Scholar]
  46. Sachsenröder J., Twardziok S., Hammerl J. A., Janczyk P., Wrede P., Hertwig S., Johne R. 2012; Simultaneous identification of DNA and RNA viruses present in pig faeces using process-controlled deep sequencing. PLoS ONE 7:e34631 [View Article][PubMed]
    [Google Scholar]
  47. Sachsenröder J., Twardziok S. O., 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:e88888 [View Article][PubMed]
    [Google Scholar]
  48. Schrader C., Schielke A., Ellerbroek L., Johne R. 2012; PCR inhibitors – occurrence, properties and removal. J Appl Microbiol 113:1014–1026 [View Article][PubMed]
    [Google Scholar]
  49. Schulz E., Gottschling M., Ulrich R. G., Richter D., Stockfleth E., Nindl I. 2012; Isolation of three novel rat and mouse papillomaviruses and their genomic characterization. PLoS ONE 7:e47164 [View Article][PubMed]
    [Google Scholar]
  50. Tonietti P. O., da Hora A. S., Silva F. D., Ferrari K. L., Brandão P. E., Richtzenhain L. J., Gregori F. 2013; Simultaneous detection of group a rotavirus in Swine and rat on a pig farm in Brazil. ScientificWorldJournal 2013:648406 [View Article][PubMed]
    [Google Scholar]
  51. Tse H., Chan W. M., Lam C. S., Lau S. K., Woo P. C., Yuen K. Y. 2012; Complete genome sequences of novel rat noroviruses in Hong Kong. J Virol 86:12435–12436 [View Article][PubMed]
    [Google Scholar]
  52. Tsugawa T., Tatsumi M., Tsutsumi H. 2014; Virulence-associated genome mutations of murine rotavirus identified by alternating serial passages in mice and cell cultures. J Virol 88:5543–5558 [View Article][PubMed]
    [Google Scholar]
  53. Victoria J. G., 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 83:4642–4651 [View Article][PubMed]
    [Google Scholar]
  54. Vonderfecht S. L., Huber A. C., Eiden J., Mader L. C., Yolken R. H. 1984; Infectious diarrhea of infant rats produced by a rotavirus-like agent. J Virol 52:94–98[PubMed]
    [Google Scholar]
  55. Wiegering V., Kaiser J., Tappe D., Weissbrich B., Morbach H., Girschick H. J. 2011; Gastroenteritis in childhood: a retrospective study of 650 hospitalized pediatric patients. Int J Infect Dis 15:e401–e407 [View Article][PubMed]
    [Google Scholar]
  56. Wolf S., Reetz J., Johne R., Heiberg A. C., Petri S., Kanig H., Ulrich R. G. 2013; The simultaneous occurrence of human norovirus and hepatitis E virus in a Norway rat (Rattus norvegicus). Arch Virol 158:1575–1578 [View Article][PubMed]
    [Google Scholar]
  57. Xie G., Yu J., Duan Z. 2013; New strategy for virus discovery: viruses identified in human feces in the last decade. Sci China Life Sci 56:688–696 [View Article][PubMed]
    [Google Scholar]
/content/journal/jgv/10.1099/vir.0.070029-0
Loading
/content/journal/jgv/10.1099/vir.0.070029-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error