Skip to main content

Ruminal Viruses (Bacteriophages, Archaeaphages)

  • Chapter
Rumen Microbiology: From Evolution to Revolution

Abstract

Viruses of prokaryotes (phages) are ubiquitous to the gastrointestinal tracts of all animals, and particularly dense and diverse populations occur in the rumen of herbivores. Although knowledge of their existence dates back to the 1960s, very few studies were undertaken until the late 1980s and 1990s, when a number of investigators examined rumen phages at both the individual and ecosystem level. Despite the fact that these viruses have characteristics that can be both detrimental (reduce feed efficiency, transfer toxin genes) and advantageous (bacterial population balance, lateral gene transfer, phage therapy, novel enzymes), very little is known about their biological properties or genetic make-up. With recent technical advances in molecular biology, particularly developments in high-throughput sequencing, the field of rumen phage research is predicted to rapidly change, with individual phage isolates and the entire virus fraction (viral metagenome or virome) being characterised in ways never previously possible. The overall importance of phage-host interactions in relation to the functioning of the rumen microbial ecosystem and the nutrition of the animal remains elusive, but these viruses are likely to impact on the bacterial population balance and the flow of genetic material between microorganisms within the ecosystem.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abedon ST (2012) Phage therapy best practices. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 256–272

    Google Scholar 

  • Ackermann HW, Dubow MS (1987a) General properties of bacteriophages. CRCPress, Boca Raton

    Google Scholar 

  • Ackermann HW, DuBow MS (1987b) Natural groups of bacteriophages. CRC Press, Boca Raton

    Google Scholar 

  • Adams JC, Gazaway JA, Brailsford MD et al (1966) Isolation of bacteriophages from the bovine rumen. Experentia 22:717–718

    Google Scholar 

  • Ambrozic J, Ferme D, Grabnar M et al (2001) The bacteriophages of ruminal prevotellas. Folia Microbiol 46:37–39

    CAS  Google Scholar 

  • Andres D, Roske Y, Doering C et al (2012) Tail morphology controls DNA release in two Salmonella phages with one lipopolysaccharide receptor recognition system. Mol Microbiol 83:1244–1253

    CAS  PubMed  Google Scholar 

  • Angly F, Rodriguez-Brito B et al (2005) PHACCS, an online tool for estimating the structure and diversity of uncultured viral communities using metagenomic information. BMC Bioinf 6:41

    Google Scholar 

  • Angly FE, Felts B et al (2006) The marine viromes of four oceanic regions. PLoS Biol 4:2121–2131

    CAS  Google Scholar 

  • Annison EF, Lewis D (1959) Metabolism in the rumen. Methuen, London

    Google Scholar 

  • Attwood GT, Kelly WJ, Altermann EH et al (2008) Analysis of the Methanobrevibacter ruminantium draft genome: understanding methanogen biology to inhibit their action in the rumen. Aust J Exp Agric 48:83–88

    CAS  Google Scholar 

  • Aziz RK, Bartels D et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75

    Google Scholar 

  • Baresi L, Bertani G (1984) Isolation of a bacteriophage for a methanogenic bacterium. Abstr Ann Meet Am Soc Microbiol 28:133

    Google Scholar 

  • Barnet YM (1972) Bacteriophages of Rhizobium trifolii I morphology and host range. J Gen Virol 15:1–15

    CAS  PubMed  Google Scholar 

  • Barrangou R (2013) CRISPR-Cas systems and RNA-guided interference. Wiley Interdiscip Rev-RNA 4:267–278

    CAS  PubMed  Google Scholar 

  • Barrangou R, Fremaux C, Deveau H et al (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712

    CAS  PubMed  Google Scholar 

  • Bentley SD, Parkhill J (2004) Comparative genomic structure of prokaryotes. Annu Rev Genet 38:771–792

    CAS  PubMed  Google Scholar 

  • Berg Miller ME, Yeoman CJ et al (2012) Phage–bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome. Environ Microbiol 14:207–227

    CAS  PubMed  Google Scholar 

  • Bird SH, Romulo B, Leng RA (1994) Effects of lucerne supplementation and defaunation on feed intake, digestibility, N-retention and productivity of sheep fed straw based diets. Anim Feed Sci Technol 45:119–129

    Google Scholar 

  • Bland C, Ramsey TL, Sabree F et al (2007) CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinf 8:209

    Google Scholar 

  • Bobay L-M, Rocha EPC, Touchon M (2013) The adaptation of temperate bacteriophages to their host genomes. Mol Biol Evol 30:737–751

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bose M, Barber RD (2006) Prophage Finder: a prophage loci prediction tool for prokaryotic genome sequences in silico. Biol 6:223–227

    CAS  Google Scholar 

  • Brailsford MD, Hartman PA (1968) Characterisation of Streptococcus durans bacteriophages. Can J Microbiol 14:397–402

    CAS  PubMed  Google Scholar 

  • Brenner S, Horne RW (1959) A negative staining method for high resolution electron microscopy of viruses. Biochim Biophys Acta 34:103–110

    CAS  PubMed  Google Scholar 

  • Brulc JM, Antonopoulos DA et al (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci U S A 106:1948–1953

    CAS  PubMed Central  PubMed  Google Scholar 

  • Callaway TR, Edrington TS et al (2008) Bacteriophage isolated from feedlot cattle can reduce Escherichia coli O157: H7 populations in ruminant gastrointestinal tracts. Foodborne Pathog Dis 5:183–191

    CAS  PubMed  Google Scholar 

  • Callaway TR, Edrington TS et al (2011) Evaluation of phage treatment as a strategy to reduce salmonella populations in growing swine. Foodborne Pathog Dis 8:261–266

    CAS  PubMed  Google Scholar 

  • Campbell AM (1992) Chromosomal insertion sites for phages and plasmids. J Bacteriol 174:7495–7499

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8:769–783

    CAS  PubMed  Google Scholar 

  • Cheong JP, Brooker JD (1998) Lysogenic bacteriophage M1 from Selenomonas ruminantium: isolation, characterisation and DNA sequence analysis of the integration site. Microbiology 144:2195–2202

    CAS  PubMed  Google Scholar 

  • Clokie MRJ, Millard AD, Letarov AV et al (2011) Phages in nature. Bacteriophage 1:31–45

    PubMed Central  PubMed  Google Scholar 

  • Cottle DJ, Nolan JV, Wiedemann SG (2011) Ruminant enteric methane mitigation: a review. Anim Prod Sci 51:491–514

    CAS  Google Scholar 

  • D’Herelle F (1918) Technique de la recherche du microbe filtrant bacteriophage (Bacteriophagum intestinale). C R Seances Soc Biol Fil 81:1160–1162

    Google Scholar 

  • Dixon RM, Nolan JV (1986) Nitrogen and carbon flows between the caecum, blood and rumen in sheep given chopped lucerne (Medicago sativa) hay. Br J Nutr 55:313–332

    CAS  PubMed  Google Scholar 

  • Donlan RM (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17:66–72

    CAS  PubMed  Google Scholar 

  • Duckworth DH (1987) History and basic properties of bacterial viruses. In: Goyal SM, Gerba CP, Bitton G (eds) Phage ecology. John Wiley and Sons Inc, New York, pp 1–44

    Google Scholar 

  • Fenton M, Ross P, McAuliffe O et al (2010) Recombinant bacteriophage lysins as antibacterials. Bioeng Bugs 1:9–16

    PubMed Central  PubMed  Google Scholar 

  • Firkins JL, Weiss WP, Piwonka EJ (1992) Quantification of intraruminal recycling of microbial nitrogen using nitrogen-15. J Anim Sci 70:3223–3233

    CAS  PubMed  Google Scholar 

  • Flewett TH, Bryden AS, Davies H (1974) Diagnostic electron microscopy of faeces. J Clin Pathol 27:603–614

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gantner S, Andersson AF, Alonso-Saez L et al (2011) Novel primers for 16S rRNA-based archaeal community analyses in environmental samples. J Microbiol Methods 84:12–18

    CAS  PubMed  Google Scholar 

  • Gill JJ, Hyman P (2010) Phage choice, isolation, and preparation for phage therapy. Curr Pharm Biotechnol 11:2–14

    CAS  PubMed  Google Scholar 

  • Gregg K, Kennedy BG, Klieve AV (1994) Cloning and DNA sequence analysis of the region containing AttP of the temperate phage AR29 of Prevotella ruminicola AR29. Microbiology 140:2109–2114

    CAS  PubMed  Google Scholar 

  • Grissa I, Vergnaud G (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52–W57

    PubMed Central  PubMed  Google Scholar 

  • Grissa I, Vergnaud G, Pourcel C (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinf 8:172

    Google Scholar 

  • Hatfull GF (2008) Bacteriophage genomics. Curr Opin Microbiol 11:447–453

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hazlewood GP, Munn EA, Orpin CG (1983) Temperate bacteriophages of Selenomonas ruminantium and a Fusobacterium sp isolated from the ovine rumen. In: Abstracts Canadian society for microbiology 33rd annual meeting, Winnipeg, Manitoba, Canada. p 76

    Google Scholar 

  • Hendrickson H (2012) The lion and the mouse: how bacteriophages create, liberate and decimate bacterial pathogens. In: Hyman P, Abedon S (eds) Bacteriophages in health and disease. CABI, Oxford

    Google Scholar 

  • Hess M, Sczyrba A et al (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467

    CAS  PubMed  Google Scholar 

  • Hong SH, Kim JS et al (2004) The genome sequence of the capnophilic rumen bacterium Mannheimia succiniciproducens. Nat Biotechnol 22:1275–1281

    CAS  PubMed  Google Scholar 

  • Hoogenraad NJ, Hird FJR, Holmes I et al (1967) Bacteriophages in rumen contents of sheep. J Gen Virol 1:575–576

    CAS  PubMed  Google Scholar 

  • Hurwitz BL, Sullivan MB (2013) The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecol. PLoS One 8:e57355

    Google Scholar 

  • Iverson WJ, Millis NF (1976a) Characterisation of Streptococcus bovis bacteriophages. Can J Microbiol 22:847–852

    CAS  PubMed  Google Scholar 

  • Iverson WJ, Millis NF (1976b) Lysogeny in Streptococcus bovis. Can J Microbiol 22:853–857

    CAS  PubMed  Google Scholar 

  • Iverson WG, Millis NF (1977) Succession of Streptococcus bovis strains with differing bacteriophage sensitivities in the rumens of two fistulated sheep. Appl Environ Microbiol 33:810–813

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jiang WH, Patterson JA, Steenson LR (1995) Isolation and characterisation of a temperate bacteriophage from a ruminal acetogen. Curr Microbiol 31:336–339

    CAS  PubMed  Google Scholar 

  • Kellenberger E (1995) History of phage research as viewed by a European. FEMS Microbiol Rev 17:7–24

    CAS  Google Scholar 

  • Kim MS, Park EJ, Roh SW et al (2011) Diversity and abundance of single-stranded DNA viruses in human feces. Appl Environ Microbiol 54:1637–1641

    Google Scholar 

  • Klieve AV (1988) Bacteriophages of rumen bacteria. PhD thesis, University of New England

    Google Scholar 

  • Klieve AV (2005) Part 2.2. Bacteriophages. In Makkar HPS, McSweeney CS (eds) Methods in gut microbial ecology for ruminants. International Atomic Energy Agency/Springer/Academic, Dordrecht, The Netherlands, pp 39–46

    Google Scholar 

  • Klieve AV, Bauchop T (1988) Morphological diversity or ruminal bacteriophages from sheep and cattle. Appl Environ Microbiol 54:1637–1641

    CAS  PubMed Central  PubMed  Google Scholar 

  • Klieve AV, Bauchop T (1991) Phage resistance and altered growth habit in a strain of Streptococcus bovis. FEMS Microbiol Lett 80:155–160

    CAS  Google Scholar 

  • Klieve AV, Gilbert RA (2005) Part 4.2. Bacteriophage populations. In: Makkar HPS, McSweeney CS (eds) Methods in gut microbial ecology for ruminants. International Atomic Energy Agency/Springer/Academic, Dordrecht, The Netherlands, pp 129–137

    Google Scholar 

  • Klieve AV, Hegarty R (1999) Opportunities for biological control of ruminal methanogenesis. Aust J Agr Res 50:1315–1319

    Google Scholar 

  • Klieve AV, Swain RA (1993) Estimating ruminal bacteriophage numbers using pulsed field gel electrophoresis and laser densitometry. Appl Environ Microbiol 59:2299–2303

    CAS  PubMed Central  PubMed  Google Scholar 

  • Klieve AV, Hudman JF, Bauchop T (1989) Inducible bacteriophages from ruminal bacteria. Appl Environ Microbiol 55:1630–1634

    CAS  PubMed Central  PubMed  Google Scholar 

  • Klieve AV, Gregg K, Bauchop T (1991) Isolation and characteristics of lytic phages from Bacteroides ruminicola ss brevis. Curr Microbiol 23:183–187

    CAS  Google Scholar 

  • Klieve AV, Turner AF, Heck GL (1998) Dietary influences on bacteriophage numbers in the rumen. Proc Aust Soc Anim Prod 22:341

    Google Scholar 

  • Klieve AV, Heck GL, Prance MA et al (1999) Genetic homogeneity and phage susceptibility of ruminal strains of Streptococcus bovis isolated in Australia. Lett Appl Microbiol 29:108–112

    CAS  PubMed  Google Scholar 

  • Klieve AV, Bain PA, Yokoyama MT et al (2004) Bacteriophages that infect the cellulolytic ruminal bacterium Ruminococcus albus AR67. Lett Appl Microbiol 38:333–338

    CAS  PubMed  Google Scholar 

  • Krupovic M, Prangishvili D, Hendrix RW et al (2011) Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol Mol Biol Rev 75:610

    PubMed Central  PubMed  Google Scholar 

  • Kuhl S, Hyman P, Abedon ST (2012) Diseases caused by phages. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 21–32

    Google Scholar 

  • Leahy SC, Kelly WJ et al (2010) The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. Plos One 5:e8926

    Google Scholar 

  • Leedle JAZ, Bryant MP, Hespell RB (1982) Diurnal variations in bacterial numbers and fluid parameters in ruminal contents of animals fed low- or high-forage diets. Appl Environ Microbiol 44:402–412

    CAS  PubMed Central  PubMed  Google Scholar 

  • Leng RA (1990) Factors affecting the utilisation of ‘poor-quality’ forages by ruminants particularly under tropical conditions. Nutr Res Rev 3:277–303

    CAS  PubMed  Google Scholar 

  • Lima-Mendez G, Van Helden J, Toussaint A et al (2008) Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 24:863–865

    CAS  PubMed  Google Scholar 

  • Lockington RA, Attwood GT, Brooker JD (1988) Isolation and characterisation of a temperate bacteriophage from the ruminal anaerobe Selenomonas ruminantium. Appl Environ Microbiol 54:1575–1580

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lood R, Collin M (2011) Characterization and genome sequencing of two Propionibacterium acnes phages displaying pseudolysogeny. BMC Genomics 12:198

    Google Scholar 

  • Markowitz VM, Chen IMA et al (2012) IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 40:D115–D122

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matteuzzi D, Sozzi T (1971) Bifidobacterium bacteriophage from calf rumen Zeitschrift fur Allgemeine. Mikrobiologie 11:57–58

    CAS  Google Scholar 

  • Monk AB, Rees CD, Barrow P (2010) Under the microscope, bacteriophage applications: where are we now? Lett Appl Microbiol 51:363–369

    CAS  PubMed  Google Scholar 

  • Morrison M, Mackie RI (1996) Nitrogen metabolism by ruminal microorganisms: current understanding and future perspectives. Aust J Agr Res 47:227–246

    Google Scholar 

  • Mumm JP, Landy A, Gelles J (2006) Viewing single lambda site-specific recombination events from start to finish. EMBO J 25:4586–4595

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murphy FA, Fauquet CM, Bishop DHL et al (1995) Virus taxonomy, 6th report of the international committee on taxonomy of viruses. Springer-Verlag, New York

    Google Scholar 

  • Nagaraja TG, Titgemeyer EC (2007) Ruminal acidosis in beef cattle: the current microbiological and nutritional outlook. J Dairy Sci 90:E17–E38

    PubMed  Google Scholar 

  • Nagaraja TG, Newbold CJ, Van Nevel CJ et al (1997) Manipulation of ruminal fermentation. In: Hobson PN, Stewart CS (eds) The rumen microbial ecosystem. Chapman and Hall, London

    Google Scholar 

  • Nemcova R, Styriak I, Stachova M et al (1993) Isolation and partial characterisation of three rumen Lactobacillus plantarum bacteriophages. Microbiologica 16:177–180

    CAS  PubMed  Google Scholar 

  • Nolan JV, Leng RA (1972) Dynamic aspects of ammonia and urea metabolism in sheep. Br J Nutr 27:177–194

    CAS  PubMed  Google Scholar 

  • O’Flaherty S, Ross RP, Coffey A (2009) Bacteriophage and their lysins for elimination of infectious bacteria. FEMS Microbiol Rev 33:801–819

    PubMed  Google Scholar 

  • O’Mahony J, Fenton M, Henry M et al (2011) Lysins to kill – a tale of viral weapons of mass destruction. Bioeng Bugs 2:306–308

    PubMed  Google Scholar 

  • Orpin CG, Munn EA (1974) The occurrence of bacteriophages in the rumen and their influence on rumen bacterial populations. Experentia 30:1018–1020

    CAS  Google Scholar 

  • Paynter MJB, Ewert DL, Chalupa W (1969) Some morphological types of bacteriophages in bovine rumen contents. Appl Microbiol 18:942–943

    CAS  PubMed Central  PubMed  Google Scholar 

  • Porter K, Russ BE, Dyall-Smith ML (2007) Virus-host interactions in salt lakes. Curr Opin Microbiol 10:418–424

    CAS  PubMed  Google Scholar 

  • Purushe J, Fouts DE, Morrison M et al (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 60:721–729

    PubMed  Google Scholar 

  • Refardt D (2011) Within-host competition determines reproductive success of temperate bacteriophages. ISME J 5:1451–1460

    PubMed Central  PubMed  Google Scholar 

  • Ritchie AE, Robinson IM, Allison MJ (1970) Rumen bacteriophage: survey of morphological types. In: Societie Francaise de Microscopie Electronique. Grenoble pp 333–334

    Google Scholar 

  • Ronning CM, Losada L, Brinkac L et al (2010) Genetic and phenotypic diversity in Burkholderia: contributions by prophage and phage-like elements. BMC Microbiol 10:202

    Google Scholar 

  • Rosario K, Breitbart M (2011) Exploring the viral world through metagenomics. Curr Opin Virol 1:289–297

    CAS  PubMed  Google Scholar 

  • Ross EM, Moate PJ, Bath CR et al (2012) High throughput whole rumen metagenome profiling using untargeted massively parallel sequencing. BMC Genet 13:53

    Google Scholar 

  • Roux S, Faubladier M, Mahul A et al (2011) Metavir: a web server dedicated to virome analysis. Bioinformatics 27:3074–3075

    CAS  PubMed  Google Scholar 

  • Roux S, Enault F, Robin A et al (2012) Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7:33641

    Google Scholar 

  • Sampson TR, Saroj SD, Llewellyn AC et al (2013) A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497:254

    CAS  PubMed Central  PubMed  Google Scholar 

  • Seet SGM (2005) Genome sequence of bacetriophage Phi-AR29: a basis for integrative plasmid vectors. PhD thesis, Murdoch University

    Google Scholar 

  • Shen Y, Mitchell M, Donovan DM et al (2012) Phage-based enzybiotics. In: Abedon S, Hyman P (eds) Bacteriophages in health and disease. CABI Press, Wallingford, Oxfordshire, UK pp 217–239

    Google Scholar 

  • Sorek R, Kunin V, Hugenholtz P (2008) CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6:181–186

    CAS  PubMed  Google Scholar 

  • Sorek R, Lawrence CM, Wiedenheft B (2013) CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu Rev Biochem 82:237–266

    CAS  PubMed  Google Scholar 

  • Stewart CS, Flint HJ, Bryant MP (1997) The rumen bacteria. In: Hobson PN, Stewart CS (eds) The rumen microbial ecosystem. Chapman and Hall, London

    Google Scholar 

  • Styriak I, Kmet V, Spanova A (1989) Isolation and characterisation of two rumen Streptococcus bovis bacteriophages. Microbiologica 12:317–322

    CAS  PubMed  Google Scholar 

  • Styriak I, Galfi P, Kmet V (1991) Preliminary observations of interaction between bacteriophages and Streptococcus bovis bacteria on ruminal epithelium primoculture. Vet Microbiol 29:281–287

    CAS  PubMed  Google Scholar 

  • Styriak I, Galfi P, Kmet V (1994a) The adherence of 3 Streptococcus-bovis strains to cells of rumen-epithelium primoculture under various conditions. Arch Anim Nutr 46:357–365

    CAS  Google Scholar 

  • Styriak I, Spanova A, Montagova H et al (1994b) Isolation and characterisation of a new ruminal bacteriophage lytic to Streptococcus bovis. Curr Microbiol 28:355–358

    Google Scholar 

  • Styriak I, Pristas P, Javorsky P (1998) Lack of surface receptors not restriction-modification system determines F4 phage resistance in Streptococcus bovis II/1. Folia Microbiol 43:35–38

    CAS  Google Scholar 

  • Styriak I, Pristas P, Javorsky P (2000) Lack of GATC sites in the genome of Streptococcus bovis bacteriophage F4. Res Microbiol 151:285–289

    CAS  PubMed  Google Scholar 

  • Swain RA, Nolan JV, Klieve AV (1996) Natural variability and diurnal fluctuations within the bacteriophage population of the rumen. Appl Environ Microbiol 62:994–997

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamada H, Harasawa R, Shinjo T (1985) Isolation of a bacteriophage in Fusobacterium necrophorum. Jpn J Vet Sci 47:483–486

    CAS  Google Scholar 

  • Tarakanov BV (1974) Lysogenic cultures of Streptococcus bovis isolated from rumen of cattle and sheep. Microbiologica 43:375–377

    CAS  Google Scholar 

  • Tarakanov BV (1976) Biological properties of Streptococcus bovis bacteriophages isolated from lysogenic cultures and sheep rumen. Microbiologiia 45:695–700

    CAS  Google Scholar 

  • Tarakanov BV (1994) Regulation of microbial processes in the rumen by bacteriophages of Streptococcus bovis. Microbiology 63:373–378 (translated from Mikrobiologiya 363, 657–667)

    Google Scholar 

  • Tarakanov BV (1996) Biology of lysogenic strains of Streptococcus bovis and virulent mutants of their temperate phages. Microbiology 65:575–580

    Google Scholar 

  • Tarakanov BV (2006) The phenomenon of bacteriophagy in the rumen of ruminants. Nauchny mir, Moscow

    Google Scholar 

  • Thurber RV, Haynes M, Breitbart M et al (2009) Laboratory procedures to generate viral metagenomes. Nat Protoc 4:470–483

    CAS  PubMed  Google Scholar 

  • Torrella F, Morita RY (1979) Evidence by electron micrographs for a high incidence of bacteriophage particles in the waters of Yaquina Bay, oregon: ecological and taxonomical implications. Appl Environ Microbiol 37:774–778

    CAS  PubMed Central  PubMed  Google Scholar 

  • Twort FW (1915) An investigation on the nature of ultra-microscopic viruses. Lancet 2:1241–1243

    Google Scholar 

  • Tyutikov FM, Bespalova IA, Rebentish BA et al (1980) Bacteriophages of methanotrophic bacteria. J Bacteriol 144:375–381

    CAS  PubMed Central  PubMed  Google Scholar 

  • Van Soest PJ (1994) Nutritional ecology of the ruminant. Cornell University Press, Ithaca

    Google Scholar 

  • Wallace RJ, Cotta MA (1988) Metabolism of nitrogen-containing compounds. In: Hobson PN (ed) The rumen microbial ecosystem. Elsevier, London, pp 217–249

    Google Scholar 

  • Watanabe K, Kodama Y, Harayama S (2001) Design and evaluation of PCR primers to amplify bacterial 16S ribosomal DNA fragments used for community fingerprinting. J Microbiol Methods 44:253–262

    CAS  PubMed  Google Scholar 

  • Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181

    CAS  PubMed  Google Scholar 

  • Wells JE, Russell JB (1996) Why do many ruminal bacteria die and lyse so quickly? J Dairy Sci 79:1487–1495

    CAS  PubMed  Google Scholar 

  • Williams AG, Coleman GS (1997) The rumen protozoa. In: Hobson PN, Stewart CS (eds) The rumen microbial ecosystem. Chapman and Hall, London, pp 73–139

    Google Scholar 

  • Zhou Y, Liang Y, Lynch KH et al (2011) PHAST: a fast phage search tool. Nucleic Acids Res 39:W347–W352

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Dedication

The authors would like to dedicate this chapter to the memory of Emeritus Professor Nancy Millis (1922–2012) who made considerable contributions to rumen phage research and the development of microbiology in Australia.

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer India

About this chapter

Cite this chapter

Gilbert, R.A., Klieve, A.V. (2015). Ruminal Viruses (Bacteriophages, Archaeaphages). In: Puniya, A., Singh, R., Kamra, D. (eds) Rumen Microbiology: From Evolution to Revolution. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2401-3_9

Download citation

Publish with us

Policies and ethics