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A metagenomic study of the rumen virome in domestic caprids

Archives of Virology volume 163, pages 3415–3419 (2018)Cite this article

A Correction to this article was published on 10 October 2018

This article has been updated

Abstract

This project sought to investigate the domestic caprid rumen virome by developing a robust viral DNA isolation and enrichment protocol (utilizing membrane filtration, ultra-centrifugation, overnight PEG treatment and nuclease treatment) and using RSD-PCR and high throughput sequencing (HTS) techniques. 3.53% of the reads obtained were analogous to those of viruses denoting Siphoviridae, Myoviridae, Podoviridae, Mimiviridae, Microviridae, Poxviridae, Tectiviridae and Marseillevirus. Most of the sequenced reads from the rumen were similar to those of phages, which are critical in maintaining the rumen microbial populations under its carrying capacity. Though identified in the rumen, most of these viruses have been reported in other environments as well. Improvements in the viral DNA enrichment and isolation protocol are required to obtain data that are more representative of the rumen virome. The 102,130 unknown reads (92.31%) for the goat and 36,241 unknown reads (93.86%) for the sheep obtained may represent novel genomes that need further study.

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Change history

  • 10 October 2018

    Unfortunately, the original article was online published with error in the results section. The error is correction by this erratum.

References

  1. Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Moller K (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68:673–690. https://doi.org/10.1128/AEM.68.2.673-690.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. White BA, Cann IKO, Kocherginskaya SA, Aminov RI, Thill LA, Mackie RI, Onodera R (1999) Molecular analysis of archaea, bacteria and eucarya communities in the rumen: review. Asian-Aust J Anim Sci 12(1):129–138. https://doi.org/10.5713/ajas.1999.129

    Article  Google Scholar 

  3. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5(10):R245–R249. https://doi.org/10.1016/S107-521(98)9010

    Article  CAS  PubMed  Google Scholar 

  4. Klieve AV, Swain RA (1993) Estimation of ruminal bacteriophage numbers by pulsed-field gel-electrophoresis and laser densitometry. Appl Environ Microbiol 59(7):2299–2303

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Berg Miller ME, Yeoman CJ, Chia N, Tringe SG, Angly FE, Edwards RA, Flint HJ, Lamed R, Bayer EA, White BA (2012) Phage–bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome. Environ Microbiol 14(1):207–227. https://doi.org/10.1111/j.1462-2920.2011.02593

    Article  CAS  PubMed  Google Scholar 

  6. Fernando BR (2012) Metagenomic analysis of microbial communities in the bovine rumen, Ph.D. thesis. Oklahoma State University, Stillwater

    Google Scholar 

  7. Jiang Y, Pei J, Xin Song X, Shao W (2007) Restriction site-dependent PCR: an efficient technique for fast cloning of new genes of microorganisms. DNA Res 14:283–290. https://doi.org/10.1093/dnares/dsm023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Patel RK, Jain M (2012) NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7(2):e30619. https://doi.org/10.1371/journal.pone.0030619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:386. https://doi.org/10.1186/1471-2105-9-386

    Article  CAS  Google Scholar 

  10. Huson DH et al (2011) Integrative analysis of environmental sequences using MEGAN 4. Genome Res 21:1552–1560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Chomczynski P, Sacchi N (1992) The single-step method of RNA isolation by acid, Guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Plunge 1(2):581–585. https://doi.org/10.1038/nprot.2006.83

    Article  CAS  Google Scholar 

  12. Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16(3):1215. https://doi.org/10.1093/nar/16.3.1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tardieu A, Bonneté F, Finet S, Vivarès D (2002) Understanding salt or PEG induced attractive interactions to crystallize biological macromolecules. Acta Crystallorgr 58:1549–1553. https://doi.org/10.1107/S0907444902014439

    Article  CAS  Google Scholar 

  14. Racaniello VR, Enquist LW (2008) Principles of virology, vol 1. Molecular biology. ASM Press, Washington, DC. ISBN 1-55581-479-4

  15. Rosseel T (2015) Genome sequencing by random priming methods for viral identification, Ph.D. thesis. Ghent University, Ghent

    Google Scholar 

  16. Alan DR, Chapman D, Dixon L, Chantrey L, Alistair C, Darby CA, Hall N (2012) Application of next-generation sequencing technologies in virology. J Gen Virol 93(Pt 9):1853–1868. https://doi.org/10.1099/vir.0.043182-0

    Article  CAS  Google Scholar 

  17. Steven RG, Pop M, DeBoy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, Gordon JI, Relman DA, Fraser-Liggett CM, Nelson KE (2006) Metagenomica analysis of the human distal gut microbiome. Science 312:1355–1359. https://doi.org/10.1126/science.1124234

    Article  CAS  Google Scholar 

  18. Rondon MR, August PR, Bettermann AD, Brady SF et al (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 66(6):2541–2547. https://doi.org/10.1128/AEM.66.6.2541-2547.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D et al (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304(5667):66–74. https://doi.org/10.1126/science.1093857

    Article  PubMed  Google Scholar 

  20. Rohwer F, Prangishvili D, Lindell D (2009) Roles of viruses in the environment. Environ Microbiol 11(11):2771–2774. https://doi.org/10.1111/j.1462-2920.2009.02101.x

    Article  PubMed  Google Scholar 

  21. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS et al (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Miller RJ, Koren S, Sutton G (2010) Assembly algorithms for next generation sequencing data. Genomics 95(6):315–327. https://doi.org/10.1016/j.ygeno.2010.03.001

    Article  CAS  PubMed  Google Scholar 

  23. Ross EM, Petrovski S, Moate SP (2013) Hayes BJ (2013) Metagenomics of rumen bacteriophage from thirteen lactating dairy cattle. BMC Microbiol 13:242. https://doi.org/10.1186/1471-2180-13-242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Madera C, Monjardin C, Suarez JE (2004) Milk contamination and resistance to processing conditions determine the fate of Lactococcus lactis bacteriophages in dairies. Appl Environ Microbiol 70:7365–7371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kleerebezem M, Boekhorst J, Van Kranenburg R, Molenaar D, Kuipers R et al (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci USA 100:1990–1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hayward AC (1993) The host of Xanthomonas. In: Swings JG, Civerolo LE (eds) Xanthomonas. Chapman and Hall, London, pp 51–54

    Google Scholar 

  27. Madigan M, Martinko T, John M (eds) (2005) Brock biology of microorganisms, 11th edn. Prentice Hall, New Jersey, pp 545–572

    Google Scholar 

  28. Khan N (2009) Acanthamoeba: biology and pathogenesis. Caister Academic Press, Norfolk, p 209

    Google Scholar 

  29. Leahy SC, Kelly WJ, Altermann E, Ronimus RS, Yeoman CJ et al (2010) The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS One 5(1):e8926. https://doi.org/10.1371/journal.pone.0008926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G et al (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467

    Article  CAS  PubMed  Google Scholar 

  31. Edwards RA, Rohwer F (2005) Viral metagenomics. Nat Rev Microbiol 3(6):504–510. https://doi.org/10.1038/nrmicro1163

    Article  CAS  PubMed  Google Scholar 

  32. Qin J, Li R, Raes J, Arumagam M, Burdorf KS et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464(7285):59–65. https://doi.org/10.1038/nature08821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mastepanov M, Sigsgaard C, Dlugokencky E (2008) Large tundra methane burst during onset of freezing. Nat Prod Lett 456:628–631

    Article  CAS  Google Scholar 

  34. Eckard RJ, Grainger C, De Klein CAM (2010) Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livest Sci 130(3):47–56. https://doi.org/10.1016/j.livsci.2010.02.010

    Article  Google Scholar 

  35. Moss AR, Jouany J-P, Newbold J (2000) Methane production by ruminants: its contribution to global warming. Ann Zootech 49(2000):231–253

    Article  CAS  Google Scholar 

  36. Martin C, Morgavi DP, Doreau M (2010) Methane mitigation in ruminants: from microbe to the farm scale. Animal 4(3):351–365

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank BecA-ILRI Hub, its staff and that of the University of Nairobi for their support.

Author information

Authors and Affiliations

  1. The University of Nairobi, Nairobi, Kenya

    Samuel Namonyo, Maina Wagacha & Lillian Wambua

  2. BecA-ILRI Hub, Nairobi, Kenya

    Samuel Namonyo, Solomon Maina & Morris Agaba

  3. The Nelson Mandela African Institute of Science and Technology, Arusha, Tanzania

    Morris Agaba

  4. International Centre for Insect Physiology and Ecology, Nairobi, Kenya

    Lillian Wambua

Authors
  1. Samuel Namonyo
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  2. Maina Wagacha
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  3. Solomon Maina
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  5. Morris Agaba
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Corresponding author

Correspondence to Samuel Namonyo.

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Funding

Funding was provided by the Africa Biosciences Challenge Fund which is financed by The Syngenta Foundation for Sustainable Agriculture, The Bill & Melinda Gates Foundation, The Australian Agency for International Development and The Swedish Ministry for Foreign Affairs through the Swedish International Development Cooperation Agency.

Conflict of interest

Samuel Namonyo, Maina Wagacha, Solomon Maina, Lillian Wambua and Morris Agaba declare that they have no conflict of interest.

Ethical approval

All the rules and guidelines in the treatment and handling of the animals used in this study were followed as outlined by the ministry of livestock (Kenya) and the International Livestock Research Institute.

Additional information

Handling Editor: Tim Skern.

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Namonyo, S., Wagacha, M., Maina, S. et al. A metagenomic study of the rumen virome in domestic caprids. Arch Virol 163, 3415–3419 (2018). https://doi.org/10.1007/s00705-018-4022-4

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  • DOI: https://doi.org/10.1007/s00705-018-4022-4

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