Bovicins: The Bacteriocins of Streptococci and Their Potential in Methane Mitigation

  • Anita Kumari Garsa
  • Prasanta Kumar Choudhury
  • Anil Kumar Puniya
  • Tejpal Dhewa
  • Ravinder Kumar Malik
  • Sudhir Kumar TomarEmail author


Bovicin is a type AII lantibiotic, possessing two β-methyllanthionine and a disulfide bridge encoded by bovA gene hitherto unknown a couple of decades ago. Bacteriocins can be useful in directly inhibiting methanogens and/or redirecting H2 to other reductive microorganisms, in particular, propionate producers or reductive acetogens. So far, the role of nisin and bovicin to suppress greenhouse gas (GHG) production under in vitro conditions has been documented. GHG emissions from ruminants are a threat to the environment, because of their role in global warming as well as in climate change. Methane (CH4) produced from livestock farming practices is a potent GHG, comprising 18% of total GHG emissions in the world. Therefore, minimizing enteric CH4 production is quite essential from both the economical livestock production as well as environment perspectives. Strategies for the abatement of CH4 have provided two-way opportunities, viz., improved livestock productivity and reduced GHG emissions. In the past, different strategies have been proposed and tested to mitigate CH4, such as the dietary composition of feeds, ionophores, antibiotics, vaccines, analogues, probiotics, and secondary metabolites of plants and fungi. However, quite a few of these strategies have been adopted at farm level due to their varied effect on animal health and/or residues on animal products. The use of bacteriocins might have potential in inhibiting methanogens in the rumen. A bacteriocin produced by Streptococcus bovis (an isolate from rumen) named bovicin HC5 has been exhibited to decrease CH4 production to an extent of 50%. In this review, authors intend to discuss the sources, structure, biochemical properties, and antimicrobial spectra of bovicins, besides the potential applications with special reference to CH4 mitigation.


Bovicin Enteric fermentation Rumen bacteria Ruminants Methanogens Methane mitigation Streptococcus bovis 



The authors express their sincere gratitude to the Director, ICAR-National Dairy Research Institute, Karnal-132001, India for providing the working facilities.

Funding Information

The author Dr. Anita Kumari Garsa gratefully acknowledges the funding agency, the University Grant Commission (UGC), New Delhi, India for providing financial support in the form of UGC Post-Doctoral Fellowship for Women.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that there is no conflict of interest.


  1. 1.
    Al emery AJA, Yousif AA, Al-Hilaly HA (2013) Isolation and characterization of Streptococcus bovis from rumen content of awassi sheep in Iraq, Al-Qadisiya. J Vet Med Sci 12(1):44–51Google Scholar
  2. 2.
    Allison MJ, Robinson IM, Dougherty RW, Bucklin JA (1975) Grain overload in cattle and sheep: changes in microbial populations in the cecum and rumen. Am J Vet Res 36:181–185PubMedGoogle Scholar
  3. 3.
    Attwood GT, Altermann E, Kelly WJ, Leahy SC, Zhang L, Morrison M (2011) Exploring rumen methanogen genomes to identify targets for methane mitigation strategies. Anim Feed Sci Technol 166:65–75CrossRefGoogle Scholar
  4. 4.
    Beauchemin K, Kreuzer M, O'Mara F, McAllister T (2008) Nutritional management for enteric methane abatement: a review. Aust J Exp Agr 48:21–27CrossRefGoogle Scholar
  5. 5.
    Brotz H, Bierbaum G, Markus A, Molitor E, Sahl HG (1995) Mode of action of the lantibiotic mersacidin: inhibition of peptidoglycan biosynthesis via a novel mechanism? Antimicrob Agents Chemother 39:714–719PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Brulc JM, Antonopoulos DA, Rincon MT, Band M, Bari A, Akraiko T, Hernandez A, Thimmapuram J, Henrissat B, Coutinho PM, Borovok I, Jindou S, Lamed R, Flint HJ, Bayer EA, White BA (2009) Gene-centric metagenomics of the fibre-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci U S A 106:1948–1953PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Callaway TR, Carneiro De Melo AMS, Russell JB (1997) The effect of nisin and monensin on ruminal fermentations in vitro. Curr Microbiol 35:90–96PubMedCrossRefGoogle Scholar
  8. 8.
    Calsamiglia S, Blanch M, Ferret A, Moya D (2012) Is subacute ruminal acidosis a pH related problem? Causes and tools for its control. Anim Feed Sci Techno1 72(1):242–250Google Scholar
  9. 9.
    Chan WW, Dehority BA (1999) Production of Ruminococcus flavifaciens growth inhibitor(s) by Ruminococcus albus. Anim Feed Sci Technol 77:61–71CrossRefGoogle Scholar
  10. 10.
    Chen M, Wolin MJ (1979) Effect of monensin and lasalocid sodium on the growth of methanogenic and rumen saccharolytic bacteria. Appl Environ Microbiol 38:72–77PubMedPubMedCentralGoogle Scholar
  11. 11.
    Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20PubMedCrossRefGoogle Scholar
  12. 12.
    Cotter PD (2014) An ‘Upp’-turn in bacteriocin receptor identification. Mol Microbiol 92:1159–1163PubMedCrossRefGoogle Scholar
  13. 13.
    de Carvalho AA, Vanetti MC, Mantovani HC (2008) Bovicin HC5 reduces thermal resistance of Alicyclobacillus acidoterrestris in acidic mango pulp. J Appl Microbiol 104:1685–1691PubMedCrossRefGoogle Scholar
  14. 14.
    de Vos WM, Kuipers OP, van der Meer JR, Siezen RJ (1995) Maturation pathway of nisin and other lantibiotics: posttranslationally modified antimicrobial peptides exported by Gram positive bacteria. Mol Microbiol 17:427–437PubMedCrossRefGoogle Scholar
  15. 15.
    Dellinger CA, Ferry JG (1984) Effect of monensin on growth and methanogenesis of Methanobacterium formicicum. Appl Environ Microbiol 48:680–682PubMedPubMedCentralGoogle Scholar
  16. 16.
    Eckard R, Grainger C, De Klein C (2010) Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livest Sci 130:47–56CrossRefGoogle Scholar
  17. 17.
    EPA (2017) Overview of greenhouse gases.
  18. 18.
    FAO (2010) Greenhouse gas emissions from the dairy sector. A life cycle assessment, RomeGoogle Scholar
  19. 19.
    Ferir G, Petrova MI, Andrei G, Huskens D, Hoorelbeke B, Snoeck R, Vanderleyden J, Balzarini J, Bartoschek S, Bronstrup M, Sussmuth RD, Schols D (2013) The lantibiotic peptide labyrinthopeptin A1 demonstrates broad anti-HIV and anti-HSV activity with potential for microbicidal applications. PLoS One 8:e64010PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Field D, Cotter P, Hill C, Ross RP (2007) Bacteriocin biosynthesis, structure, and function, in research and applications in bacteriocins. Riley MA, Gillor O (Eds.):5–41Google Scholar
  21. 21.
    Fox JL (2002) APUA, Senate Bill urge restricted use of antibiotics in agriculture. ASM News 68:316–317Google Scholar
  22. 22.
    Garry F, McConnel C (2009) Indigestion in ruminants. In: Smith BP (ed) Large animal internal medicine, 3rd edn. Mosby, pp 824–830Google Scholar
  23. 23.
    Garsa AK, Kumariya R, Sood SK, Kumar A, Kapila S (2014) Bacteriocin production and different strategies for their recovery and purification. Prob Antimicrob Prot 6:47e58Google Scholar
  24. 24.
    Ghali MB, Scott PT, Al Jassim RAM (2004) Characterization of Streptococcus bovis from the rumen of the dromedary camel and Rusa deer. Lett Appl Microbiol 39(4):341–346PubMedCrossRefGoogle Scholar
  25. 25.
    Ghali MB, Scott PT, Alhadrami GA, Al-Jassim RAM (2011) Identification and characterization of the predominant lactic acid producing and lactic acid-utilizing bacteria in the foregut of the feral camel (Camelus dromedarius) in Australia. Anim Prod Sci 51(7):597–604CrossRefGoogle Scholar
  26. 26.
    Gill M, Smit P, Wilkinson JM (2010) Mitigating climate change: the role of domestic livestock. Animal 4:323–333PubMedCrossRefGoogle Scholar
  27. 27.
    GOI, 17th Livestock Census (2012) Ministry of agriculture, Government of India, February 29, 2012Google Scholar
  28. 28.
    Gravesen A, Jydegaard Axelsen AM, Mendes da Silva J, Hansen TB, Knochel S (2002) Frequency of bacteriocin resistance development and associated fitness costs in Listeria monocytogenes. Appl Environ Microbiol 68:756–764PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Gravesen A, Ramnath M, Rechinger KB, Andersen N, Jansch L, Hechard Y, Hastings JW, Knochel S (2002) High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiology 148:2361–2369PubMedCrossRefGoogle Scholar
  30. 30.
    Guo TJ, Wang JQ, Bu DP, Liu KL, Wang JP, Li D, Luan SY (2010) Evaluation of the microbial population in ruminal fluid using real time PCR in steers treated with virginiamycin. Czech J Animal Sci 55(7):276–285CrossRefGoogle Scholar
  31. 31.
    Heng NCK, Tagg JR (2006) What’s in a name? Class distinction for bacteriocins. Nat Rev Microbiol 4:160CrossRefGoogle Scholar
  32. 32.
    Heng NCK, Wescombe PA, Burton JP, Jack RW, Tagg JR (2007) The diversity of bacteriocins in Gram-positive bacteria. In: Riley MA, Chavan M (eds) Bacteriocins: ecology and evolution. Springer, Berlin, Germany, pp 45–92CrossRefGoogle Scholar
  33. 33.
    Hess M, Sczybra A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM (2011) Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467PubMedCrossRefGoogle Scholar
  34. 34.
    Holo H, Nilssen O, Nes IF (1991) Lactococcin A, a new bacteriocin from Lactococcus lactis subsp. cremoris: isolation and characterization of the protein and its gene. J Bacteriol 173:3879–3887PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Hook SE, Wright AD, McBride BW (2010) Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010(945785):1–11Google Scholar
  36. 36.
    Houlihan AJ, Russell JB (2006) Factors affecting the activity of bovicin HC5, a bacteriocin from Streptococcus bovis HC5: release, stability and binding to target bacteria. J Appl Microbiol 100:168–174PubMedCrossRefGoogle Scholar
  37. 37.
    Hungate RE (1969) A roll tube method for cultivation of strict anaerobes. In: Norris JR, Ribbons DW (eds) Methods in microbiology, vol 3B. Academic Press, London, pp 117–132Google Scholar
  38. 38.
    Hungate RE, Dougherty RW, Bryant MP, Cello RM (1952) Microbiological and physiological changes associated with acute indigestion in sheep. Cornell Vet 42:423–449PubMedPubMedCentralGoogle Scholar
  39. 39.
    Hungate RE, Smith W, Bauchop T, Yu I, Rabinowitz JC (1970) Formate as an intermediate in the bovine rumen fermentation. J Bacteriol 102:389–397PubMedPubMedCentralGoogle Scholar
  40. 40.
    Iverson WG, Mills NF (1976) Bacteriocins of Streptococcus bovis. Can J Microbiol 22:1040–1047PubMedCrossRefGoogle Scholar
  41. 41.
    Jarvis GN, Kuntovic A, Hay AG, Russell JB (2000) The physiological and genetic diversity of bovine Streptococcus bovis strains. FEMS Microbial Ecol 35:49–56Google Scholar
  42. 42.
    Jung G (1991) Lantibiotics—ribosomally synthesized biologically active polypeptides containing sulfide bridges and α, β-didehydroamino acids. Angew Chem Int Ed Engl 30:1151–1192CrossRefGoogle Scholar
  43. 43.
    Kalmokoff ML, Lu D, Whitford MF, Teather RM (1999) Evidence for production of a new lantibiotic (butyrivibriocin OR79A) by the ruminal anaerobe Butyrivibrio fibrisolvens OR79: characterization of the structural gene encoding butyrivibriocin OR79A. Appl Environ Microbiol 65:2128–2135PubMedPubMedCentralGoogle Scholar
  44. 44.
    Kalmokoff ML, Teather RM (1997) Isolation and characterization of a bacteriocin (butyrivibriocin AR10) from the ruminal anaerobe Butyrivibrio fibrisolvens AR10: evidence in support of the widespread occurrence of bacteriocin-like activity among ruminal isolates of B. fibrisolvens. Appl Environ Microbiol 63:394–402PubMedPubMedCentralGoogle Scholar
  45. 45.
    Kamra DN (2005) Rumen microbial ecosystem. Curr Sci 89(1):124–135Google Scholar
  46. 46.
    Key N, Tallard G (2012) Mitigating methane emissions from livestocks: a global analysis of sector policies. Clim Chang 112:387–414CrossRefGoogle Scholar
  47. 47.
    Kjos M, Oppegard C, Diep DB, Nes IF, Veening JW, Nissen-Meyer J, Kristensen T (2014) Sensitivity to the two-peptide bacteriocin lactococcin G is dependent on UppP, an enzyme involved in cell-wall synthesis. Mol Microbiol 92:1177–1187PubMedCrossRefGoogle Scholar
  48. 48.
    Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39–85PubMedCrossRefGoogle Scholar
  49. 49.
    Klieve AV, Heck GL, Prance MA, Shu G (1999) Genetic homogeneity and phage susceptibility of ruminal strains of Streptococcus bovis isolated in Australia. Lett Appl Microbiol 29:108–112PubMedCrossRefGoogle Scholar
  50. 50.
    Kobayashi Y (2010) Abatement of methane production from ruminants: trends in the manipulation of rumen fermentation. Asian-Aust J Anim Sci 23(3):410–416CrossRefGoogle Scholar
  51. 51.
    Kumar S, Choudhury PK, Carro MD, Griffith GW, Dagar SS, Puniya M, Calabro S, Ravella SR, Dhewa T, Upadhyay RC, Sirohi SK, Kundu SS, Wanapat M, Puniya AK (2014) New aspects and strategies for methane mitigation from ruminants. Appl Microbiol Biotechnol 98:31–44Google Scholar
  52. 52.
    Kumar S, Dagar SS, Hadi S, Ebrahimi MRK, Upadhyay RC, Puniya AK (2014) Prospective use of bacteriocinogenic Pediococcus pentosaceus as direct-fed microbial having methane reducing potential. J Integ Agric 14(3):561–566CrossRefGoogle Scholar
  53. 53.
    Kumar S, Dagar SS, Sirohi SK, Upadhyay RC, Puniya AK (2013) Microbial profiles, methanogenesis and digestibility in vitro on varying concentrations of roughages. Ann Microbiol 63:541–545CrossRefGoogle Scholar
  54. 54.
    Kumar S, Puniya AK, Puniya M, Dagar S, Sirohi S, Singh K, Griffith G (2009) Factors affecting rumen methanogens and methane mitigation strategies. World J Microbiol Biotechnol 25:1557–1566CrossRefGoogle Scholar
  55. 55.
    Kumariya R, Sood SK, Rajput YS, Garsa AK (2014) Gradual pediocin PA-1 resistance in Enterococcus faecalis confers cross-protection to diverse pore-forming cationic antimicrobial peptides displaying changes in cell wall and mannose PTS expression. Ann Microbiol 65:721–732CrossRefGoogle Scholar
  56. 56.
    Kupke T, Gotz F (1996) Post-translational modifications of lantibiotics. Antonie Van Leeuwenhoek 69:139–150PubMedCrossRefGoogle Scholar
  57. 57.
    Leahy SC, Kelly WJ, Altermann E, Ronimus RS, Yeoman CJ, Pacheco DM, Li D, Kong Z, McTavish S, Sang C (2010) The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS One 5:e8926PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Leahy SC, Kelly WJ, Li D, Altermann E, Lambie SC, Cox F, Attwood GT (2013) The complete genome sequence of Methanobrevibacter sp. AbM4. Stand Genomic Sci 8:2CrossRefGoogle Scholar
  59. 59.
    Lee JH, Rhee MS, Kumar S, Lee GH, Kim DS, Choi SH, Lee DW, Yoon MH, Kim BC (2013) Genome sequence of a Methanobreibacter sp. strain JH1 isolated from the rumen of Korean native cattle. Genome Announcement 1:e00002–e00013. CrossRefGoogle Scholar
  60. 60.
    Lee SS, Hsu JT, Mantovani HC, Russell JB (2002) The effect of bovicin HC5, a bacteriocin from Streptococcus bovis HC5, on ruminal methane production in vitro. FEMS Microbiol Lett 217:51–55PubMedCrossRefGoogle Scholar
  61. 61.
    Mantovani HC, Hu H, Worobo RW, Russell JB (2002) Bovicin HC5, a bacteriocin from Streptococcus bovis HC5. Microbiology 148:3347–3352PubMedCrossRefGoogle Scholar
  62. 62.
    Mantovani HC, Kam DK, Ha JK, Russell JB (2001) The antibacterial activity and sensitivity of Streptococcus bovis strains isolated from the rumen of cattle. FEMS Microbiol Ecol 37:223–229Google Scholar
  63. 63.
    Mantovani HC, Russell JB (2001) Nisin resistance of Streptococcus bovis. Appl Environ Microbiol 67:808–813PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Mantovani HC, Russell JB (2003) Inhibition of Listeria monocytogenes by bovicin HC5, a bacteriocin produced by Streptococcus bovis HC5. Int J Food Microbiol 89:77–83PubMedCrossRefGoogle Scholar
  65. 65.
    Mantovani HC, Russell JB (2008) Bovicin HC5, a lantibiotic produced by Streptococcus bovis HC5, catalyzes the efflux of intracellular potassium but not ATP. Antimicrob Agents Chemother 52(6):2247–2249PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Maqueda M, Gálvez A, Sánchez-Barrena MJ, González C, Albert A, Rico M, Valdivia E (2004) Peptide AS-48: prototype of a new class of cyclic bacteriocins. Curr Prot Pept Sci 5:399–416CrossRefGoogle Scholar
  67. 67.
    Martin C, Morgavi DP, Doreau M (2010) Methane mitigation in ruminants: from microbe to the farm scale. Animal 4:351–365PubMedCrossRefGoogle Scholar
  68. 68.
    McAllister TA, Newbold CJ (2008) Redirecting rumen fermentation to reduce methanogenesis. Aust J Exp Agric 48:7–13CrossRefGoogle Scholar
  69. 69.
    Morgavi DP, Kelly WJ, Janssen PH, Attwood GT (2013) Rumen microbial (meta) genomics and its application to ruminant production. Animal 7:184–201PubMedCrossRefGoogle Scholar
  70. 70.
    Morovsky M, Pristas S, Czikkova JP (1998) A bacteriocin mediated antagonism by Enterococcus faecium BC25 against ruminal Streptococcus bovis. Microbiol Res 153:277–281PubMedCrossRefGoogle Scholar
  71. 71.
    Moss AR, Jouany JP, Newbold J (2000) Methane production by ruminants: its contribution to global warming. Ann Zootech 49:231–254CrossRefGoogle Scholar
  72. 72.
    Muller WM, Ensle P, Krawczyk B, Sussmuth RD (2011) Leader-peptide directed processing of labyrinthopeptin A2 precursor peptides by the modifying enzyme LabKC. Biochem 50:8362–8373CrossRefGoogle Scholar
  73. 73.
    Murphy K, O’Sullivan O, Rea MC, Cotter PD, Ross RP, Hill C (2011) Genome mining for radical SAM protein determinants reveal multiple sactibiotic-like gene clusters. PLoS One 6:e20852PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Odenyo AA, Mackie RI, Stahl DA, White BA (1994) The use of 16S rRNA-targeted oligonucleotide probes to study competition between ruminal fibrolytic bacteria: development of probes for Ruminococcus species and evidence for bacteriocin production. Appl Environ Microbiol 60:3688–3696PubMedPubMedCentralGoogle Scholar
  75. 75.
    Paik SH, Chakicherla A, Hansen JN (1998) Identification and characterization of the structural and transporter genes for, and the chemical and biological properties of, sublancin 168, a novel lantibiotic produced by Bacillus subtilis 168. J Biol Chem 273:23134–23142PubMedCrossRefGoogle Scholar
  76. 76.
    Paiva AD, Breukink E, Mantovani HC (2011) Role of lipid II and membrane thickness in the mechanism of action of the lantibiotic bovicin HC5. Antimicrob Agents Chemother 55:5284–5293PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Paiva AD, Fernandes KM, Dias RS, Rocha AS, de Oliveira LL, Neves CA, de Paula SO, Mantovani HC (2013) Safety evaluation of the antimicrobial peptide bovicin HC5 orally administered to a murine model. BMC Microbiol 13(1):69–80PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Paiva AD, Oliveira MD, de Paula SO, Baracat-Pereira MC, Breukink E, Mantovani HC (2012) Toxicity of bovicin HC5 against mammalian cell lines and the role of cholesterol in bacteriocin activity. Microbiology 158:2851–2858PubMedCrossRefGoogle Scholar
  79. 79.
    Pandey N, Malik RK, Kaushik JK, Singroha G (2013) Gassericin A: a circular bacteriocin produced by lactic acid bacteria Lactobacillus gasseri. World J Microbiol Biotechnol 29:1977–1987PubMedCrossRefGoogle Scholar
  80. 80.
    Patra AK (2012) Enteric methane mitigation technologies for ruminant livestock: a synthesis of current research and future directions. Environ Monit Assess 184:1929–1952PubMedCrossRefGoogle Scholar
  81. 81.
    Radositis OM, Gay CC, Hinchliff KW, Connstable PD (2007) Veterinary medicine: a textbook of the disease of cattle, horses, sheep, pigs and goats, 10th edn. Elsevier Saunders, London, pp 966–994Google Scholar
  82. 82.
    Russell JB, Mantovani HC (2002) The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. J Mol Microbiol Biotechnol 4:347–355PubMedGoogle Scholar
  83. 83.
    Russell JB, Strobel HJ (1989) Mini-review: the effect of ionophores on ruminal fermentation. Appl Environ Microbiol 55:1–6PubMedPubMedCentralGoogle Scholar
  84. 84.
    Sahl HG, Jack RW, Bierbaum G (1995) Biosynthesis and biological activities of lantibiotics with unique post-translational modifications. Eur J Biochem 230:827–853PubMedCrossRefGoogle Scholar
  85. 85.
    Sakayori Y, Muramatsu M, Hanada S, Kamagata Y, Kawamoto S, Shima J (2003) Characterization of Enterococcus faecium mutants resistant to mundticin KS, a class IIa bacteriocin. Microbiology 149:2901–2908PubMedCrossRefGoogle Scholar
  86. 86.
    Scheehle EA, Kruger D (2006) Global anthropogenic methane and nitrous oxide emissions. The Energy J 22:33–44Google Scholar
  87. 87.
    Schlegel L, Grimont R, Ageron E, Grimont PAD, Bouvet A (2003) Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonicus subsp. nov. and S. gallolyticus subsp. pasteurianus subsp. nov. Int J Syst Evol Microbiol 53(3):631–645PubMedCrossRefGoogle Scholar
  88. 88.
    Teather RM, Forster RJ (1998) Manipulating the rumen microflora with bacteriocins to improve ruminant production. Canad J Ani Sci 78:57–69CrossRefGoogle Scholar
  89. 89.
    Thorpe A (2009) Enteric fermentation and ruminant eructation: the role (and control?) of methane in the climate change debate. Clim Chang 93:407–431CrossRefGoogle Scholar
  90. 90.
    Twomey D, Ross RP, Ryan M, Meaney B, Hill C (2002) Lantibiotics produced by lactic acid bacteria: structure, function and applications. Antonie Van Leeuwenhoek 82:165–185PubMedCrossRefGoogle Scholar
  91. 91.
    Uzelac G, Kojic M, Lozo J, Aleksandrzak-Piekarczyk T, Gabrielsen C, Kristensen T, Nes IF, Diep DB, Topisirovic L (2013) A Zn-dependent metallopeptidase is responsible for sensitivity to LsbB, a class II leaderless bacteriocin of Lactococcus lactis subsp. lactis BGMN1-5. J Bacteriol 195:5614–5621PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    van Kraaij C, de Vos WM, Siezen RJ, Kuipers OP (1999) Lantibiotics: biosynthesis, mode of action and applications. Nat Prod Rep 16:575–587PubMedCrossRefGoogle Scholar
  93. 93.
    Van Nevel CJ, Demeyer DI (1977) Effect of monensin on rumen metabolism in vitro. Appl Environ Microbiol 34:251–257PubMedPubMedCentralGoogle Scholar
  94. 94.
    Van Nevel CJ, Demeyer DI (1995) Feed additives and other interventions for decreasing methane emissions. In: Wallace RJ, Chesson A (eds) Biotechnology in animal feeds and animal feeding, VCH. Weinheim, pp 329–349Google Scholar
  95. 95.
    Wakita M, Masuda T, Hoshino S (1986) Effect of salinomycin on the gas production by sheep rumen contents in vitro. J Anim Physiol Anim Nutr 56:243–251CrossRefGoogle Scholar
  96. 96.
    Wanapat M, Kongmun P, Poungchompu O, Cherdthong A, Khejornsart P, Pilajun R, Kaenpakdee S (2012) Effects of plants containing secondary compounds and plant oils on rumen fermentation and ecology. Trop Anim Health Prod 44:399–405PubMedCrossRefGoogle Scholar
  97. 97.
    Wang J, Ma H, Ge X, Zhang J, Teng K, Sun Z, Zhong J (2014) Bovicin HJ50-like lantibiotics, a novel subgroup of lantibiotics featured by an indispensable disulfide bridge. PLoS One 9(5):e97121PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Ward DJ, Somkuti GA (1995) Characterization of a bacteriocin produced by Streptococcus thermophilus ST134. Appl Microbiol Biotechnol 43:330–335PubMedCrossRefGoogle Scholar
  99. 99.
    Whitford MF, McPherson MA, Forster RJ, Teather RM (2001) Identification of bacteriocin-like inhibitors from rumen Streptococcus spp. and isolation and characterization of bovicin 255. Appl Environ Microbiol 67:569–574PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Xavier BM, Russell JB (2009) The ability of non-bacteriocin producing Streptococcus bovis strains to bind and transfer bovicin HC5 to other sensitive bacteria. Anaerobe 15:168–172PubMedCrossRefGoogle Scholar
  101. 101.
    Xiao H, Chen X, Chen M, Tang S, Zhao X, Huan L (2004) Bovicin HJ50, a novel lantibiotic produced by Streptococcus bovis HJ50. Microbiology 150:103–108PubMedCrossRefGoogle Scholar
  102. 102.
    Yang SC, Lin CH, Sung CT, Fang JY (2014) Antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front Microbiol 241(5):1–10Google Scholar
  103. 103.
    Zacharof MP, Lovitt RW (2012) Bacteriocin produced by lactic acid bacteria: a review article. APCBEE Proc 2:50–56CrossRefGoogle Scholar
  104. 104.
    Zhang J, Feng Y, Teng K, Lin Y, Gao Y, Wang J, Zhong J (2014) Type AII lantibiotic bovicin HJ50 with a rare disulfide bond: structure, structure–activity relationships and mode of action. Biochem J 461(3):497–508PubMedCrossRefGoogle Scholar
  105. 105.
    Zhou YY, Mao HL, Jiang F, Wang JK, Liu JX, McSweeney CS (2011) Inhibition of rumen methanogenesis by tea saponins with reference to fermentation pattern and microbial communities in Hu sheep. Anim Feed Sci Technol 166:93–100CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Anita Kumari Garsa
    • 1
  • Prasanta Kumar Choudhury
    • 1
    • 2
  • Anil Kumar Puniya
    • 1
    • 3
  • Tejpal Dhewa
    • 4
  • Ravinder Kumar Malik
    • 1
  • Sudhir Kumar Tomar
    • 1
  1. 1.Dairy Microbiology DivisionICAR-National Dairy Research InstituteKarnalIndia
  2. 2.Animal Nutrition DivisionICAR-National Dairy Research InstituteKarnalIndia
  3. 3.College of Dairy Science & TechnologyGuru Angad Dev Veterinary and Animal Sciences UniversityLudhianaIndia
  4. 4.Department of Nutrition BiologyCentral University of HaryanaMahendergarhIndia

Personalised recommendations