The use of direct-fed microbials for mitigation of ruminant methane emissions: A review

Animal

Volumn 8, Issue 2, 2014, Pages 250-261

  Jeyanathan, J ^a,b   Martin, C ^a,b   Morgavi, D P ^a,b  

^a UMR1213 HERBIVORES   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

biochemical pathways; direct fed microbials; methane; rumen

Indexed keywords

BOVIDAE; SACCHAROMYCES CEREVISIAE;

METHANE; PROBIOTIC AGENT; PROPIONIC ACID DERIVATIVE; SUCCINIC ACID;

ANIMAL; BACTERIUM; BIOLOGICAL MODEL; BIOSYNTHESIS; BOVIDS; DIGESTION; DRUG EFFECT; GREENHOUSE EFFECT; METABOLISM; PHYSIOLOGY; REVIEW; SACCHAROMYCES CEREVISIAE;

ANIMALS; BACTERIA; BIOSYNTHETIC PATHWAYS; DIGESTION; GLOBAL WARMING; METHANE; MODELS, BIOLOGICAL; PROBIOTICS; PROPIONATES; RUMINANTS; SACCHAROMYCES CEREVISIAE; SUCCINIC ACID;

EID: 84892801840     PISSN: 17517311     EISSN: 1751732X     Source Type: Journal    
DOI: 10.1017/S1751731113002085     Document Type: Review

References (124)

1. Adams MC, Luo J, Rayward D, King S, Gibson R and Moghaddam GH 2008. Selection of a novel direct-fed microbial to enhance weight gain in intensively reared calves. Animal Feed Science and Technology 145, 41-52.
2. Aikman PC, Henning PH, Humphries DJ and Horn CH 2011. Rumen pH and fermentation characteristics in dairy cows supplemented with Megasphaera elsdenii NCIMB 41125 in early lactation. Journal of Dairy Science 94, 2840-2849.
3. Alaboudi AR and Jones GA 1985. Effect of acclimation to high nitrate intakes on some rumen fermentation parameters in sheep. Canadian Journal of Animal Science 65, 841-849.
4. Anderson RC and Rasmussen MA 1998. Use of a novel nitrotoxin-metabolizing bacterium to reduce ruminal methane production. Bioresource Technology 64, 89-95.
5. Ao RAL 2008. The potentail of feeding nitrate to reduce enteric methane production in ruminants. A report to the department of climate change, Canberra, Australia.
6. Asa R, Tanaka A, Uehara A, Shinzato I, Toride Y, Usui N, Hirakawa K and Takahashi J 2010. Effects of protease-resistant antimicrobial substances produced by lactic acid bacteria on rumen methanogenesis. Asian-Australasian Journal of Animal Science 23, 700-707.
7. Asanuma N, Yoshii T and Hino T 2003. Isolation of new nitrite-reducing bacteria, and augmentation of nitrite reduction in the rumen by introducing one of the isolated bacteria. Bulletin of the Faculty of Agriculture-Meiji University 137, 1-17.
8. Asanuma N, Kanagawa K, Iwamoto M and Hino T 1998. Formate metabolism by ruminal microorganisms in relation to methanogenesis. Animal Science and Technology 69, 576-584.
9. Asanuma N, Iwamoto M, Kawato M and Hino T 2002. Numbers of nitratereducing bacteria in the rumen as estimated by competitive polymerase chain reaction. Animal Science Journal 73, 199-205.
10. Baldwin RL, Wood WA and Emery RS 1963. Conversion of glucose-C14 to propionate by the rumen microbiota. Journal of Bacteriology 85, 1346-1349.
11. Boccazzi P and Patterson JA 1996. Potential for functional replacement of methanogenic bacteria by acetogenic bacteria in the rumen environment. Annales De Zootechnie 45, 321.
12. Boccazzi P and Patterson JA 2011. Using hydrogen-limited anaerobic continuous culture to isolate low hydrogen threshhold ruminal acetogenic bacteria. Agriculture, Food and Analytical Bacteriology 1, 33-44.
13. Breznak JA and Switzer JM 1986. Acetate synthesis from H(2) plus CO(2) by termite gut microbes. Applied and Environmental Microbiology 52, 623-630.
14. Bryant MP 1973. Nutritional requirements of the predominant rumen cellulolytic bacteria. Federation Proceedings 32, 1809-1813.
15. Bryant MP, Campbell LL, Reddy CA and Crabill MR 1977. Growth of Desulfovibrio in lactate or ethanol media low in sulfate in association with H2-utilizing methanogenic bacteria. Applied and Environmental Microbiology 33, 1162-1169.
16. Buddle BM, Denis M, Attwood GT, Altermann E, Janssen PH, Ronimus RS, Pinares-Patiño CS, Muetzel S and Wedlock DN 2011. Strategies to reduce methane emissions from farmed ruminants grazing on pasture. The Veterinary Journal 188, 11-17.
17. Callaway TR, DeMelo AMS and Russell JB 1997. The effect of nisin and monensin on ruminal fermentations in vitro. Current Microbiology 35, 90-96.
18. Campbell LL and Postgate JR 1965. Classification of the spore-forming sulfatereducing bacteria. Bacteriological Reviews 29, 359-363.
19. Carro MD, Lebzien P and Rohr K 1992. Influence of yeast culture on the in vitro fermentation (Rusitec) of diets containing variable portions of concentrates. Animal Feed Science and Technology 37, 209-220.
20. Chaucheyras-Durand F, Walker ND and Bach A 2008. Effects of active dry yeasts on the rumen microbial ecosystem: past, present and future. Animal Feed Science and Technology 145, 5-26.
21. Chaucheyras-Durand F, Fonty G, Bertin G and Gouet P 1995. In vitro H2 utilization by a ruminal acetogenic bacterium cultivated alone or in association with an archaea methanogen is stimulated by a probiotic strain of Saccharomyces cerevisiae. Applied and Environmental Microbiology 61, 3466-3467.
22. Chaucheyras-Durand F, Masseglia S, Fonty G and Forano E 2010. Influence of the composition of the cellulolytic flora on the development of hydrogenotrophic microorganisms, hydrogen utilization, and methane production in the rumens of gnotobiotically reared lambs. Applied and Environmental Microbiology 76, 7931-7937.
23. Cheng KJ and Wallace RJ 1979. Mechanism of passage of endogenous urea through the rumen wall and the role of ureolytic epithelial bacteria in the urea flux. British Journal of Nutrition 42, 553-557.
24. Chung YH, Walker ND, McGinn SM and Beauchemin KA 2011. Differing effects of 2 active dried yeast (Saccharomyces cerevisiae) strains on ruminal acidosis and methane production in non-lactating dairy cows. Journal of Dairy Science 94, 2431-2439.
25. Counotte GH, Prins RA, Janssen RH and Debie MJ 1981. Role of Megasphaera elsdenii in the fermentation of dl-[2-C] lactate in the rumen of dairy cattle. Applied and Environmental Microbiology 42, 649-655.
26. Cummings BA, Caldwell DR, Gould DH and Hamar DW 1995. Rumen microbial alterations associated with sulfide generation in steers with dietary sulfate-induced polioencephalomalacia. American Journal of Veterinary Research 56, 1390-1395.
27. Dehority BA 1971. Carbon dioxide requirement of various species of rumen bacteria. Journal of Bacteriology 105, 70-76.
28. Dehority BA and Tirabasso PA 1998. Effect of ruminal cellulolytic bacterial concentrations on in situ digestion of forage cellulose. Journal of Animal Science 76, 2905-2911.
29. Doré J, Morvan B, Rieu-Lesme F, Goderel I, Gouet P and Pochart P 1995. Most probable number enumeration of H2-utilizing acetogenic bacteria from the digestive tract of animals and man. FEMS Microbiology Letters 130, 7-12.
30. Doreau M and Jouany JP 1998. Effect of a Saccharomyces cerevisiae culture on nutrient digestion in lactating dairy cows. Journal of Dairy Science 81, 3214-3221.
31. Dridi B, Fardeau ML, Ollivier B, Raoult D and Drancourt M 2012. Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. International Journal of Systematic and Evolutionary Microbiology 62, 1902-1907.
32. Droge S, Limper U, Emtiazi F, Schonig I, Pavlus N, Drzyzga O, Fischer U and Konig H 2005. In vitro and in vivo sulfate reduction in the gut contents of the termite Mastotermes darwiniensis and the rose-chafer Pachnoda marginata. Journal of General Applied Microbiology 51, 57-64.
33. Ellis JE, McIntyre PS, Saleh M, Williams AG and Lloyd D 1991. Influence of CO2 and low concentrations of O2 on fermentative metabolism of the ruminal ciliate Polyplastron multivesiculatum. Applied and Environmental Microbiology 57, 1400-1407.
34. Fonty G, Joblin K, Chavarot M, Roux R, Naylor G and Michallon F 2007. Establishment and development of ruminal hydrogenotrophs in methanogen-free lambs. Applied and Environmental Microbiology 73, 6391-6403.
35. Franzolin R, St-Pierre B, Northwood K and Wright AD 2012. Analysis of rumen methanogen diversity in water buffaloes (Bubalus bubalis) under three different diets. Microbial Ecology 64, 131-139.
36. Gagen EJ, Mosoni P, Denman SE, Al Jassim R, McSweeney CS and Forano E 2012. Methanogen colonisation does not significantly alter acetogen diversity in lambs isolated 17 h after birth and raised aseptically. Microbial Ecology 64, 628-640.
37. Gagen EJ, Denman SE, Padmanabha J, Zadbuke S, Al Jassim R, Morrison M and McSweeney CS 2010. Functional gene analysis suggests different acetogen populations in the bovine rumen and Tammar wallaby forestomach. Applied and Environmental Microbiology 76, 7785-7795.
38. Garcia-de-Lomas J, Corzo A, Portillo MC, Gonzalez JM, Andrades JA, Saiz-Jimenez C and Garcia-Robledoa E 2007. Nitrate stimulation of indigenous nitrate-reducing, sulfide-oxidising bacterial community in wastewater anaerobic biofilms. Water Research 41, 3121-3131.
39. Ghorbani GR, Morgavi DP, Beauchemin KA and Leedle JAZ 2002. Effects of bacterial direct-fed microbials on ruminal fermentation, blood variables, and the microbial populations of feedlot cattle. Journal of Animal Science 80, 1977-1985.
40. Gibson GR, Macfariane GT and Cummings JH 1993. Sulphate reducing bacteria and hydrogen metabolism in the large intestine. Gut 34, 437-439.
41. Godoy-Vitorino F, Goldfarb KC, Karaoz U, Leal S, Garcia-Amado MA, Hugenholtz P, Tringe SG, Brodie EL and Dominguez-Bello MG 2012. Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows. ISME Journal 6, 531-541.
42. Hallam SJ, Girguis PR, Preston CM, Richardson PM and DeLong EF 2003. Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea. Applied and Environmental Microbiology 69, 5483-5491.
43. Henning PH, Horn CH, Leeuw KJ, Meissner HH and Hagg FM 2010. Effect of ruminal administration of the lactate-utilizing strain Megasphaera elsdenii (Me) NCIMB 41125 on abrupt or gradual transition from forage to concentrate diets. Animal Feed Science and Technology 157, 20-29.
44. Hino T, Shimada K and Maruyama T 1994. Substrate preference in a strain of Megasphaera elsdenii, a ruminal bacterium, and its implications in propionate production and growth competition. Applied and Environmental Microbiology 60, 1827-1831.
45. Hou S, Makarova KS, Saw JHW, Senin P, Ly BV, Zhou Z, Ren Y, Wang J, Galperin MY, Omelchenko V, Wolf YI, Yutin N, Koonin EV, Stott B, Mountain BW, Crowe MA, Smirnova AV, Dunfield PF, Feng L, Wang L and Alam M 2008. Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biology Direct 3, 26-51. doi: 10.1186/1745-6150-3-26, published online by BioMed central 01 July 2008.
46. Hubert C and Voordouw G 2007. Oil field souring control by nitrate-reducing Sulfurospirillum spp. that outcompete sulfate-reducing bacteria for organic electron donors. Applied and Environmental Microbiology 73, 2644-2652.
47. Huisingh J, McNeill JJ and Matrone G 1974. Sulfate reduction by a Desulfovibrio species isolated from sheep rumen. Applied Microbiology 28, 489-497.
48. Hulshof RBA, Berndt A, Gerrits WJJ, Dijkstra J, van Zijderveld SM, Newbold JR and Perdok HB 2012. Dietary nitrate supplementation reduces methane emission in beef cattle fed sugarcane-based diets. Journal of Animal Science 90, 2317-2323.
49. Hungate RE, Smith W, Bauchop T, Yu I and Rabinowitz JC 1970. Formate as an intermediate in the bovine rumen fermentation. Journal of Bacteriology 102, 389-397.
50. Hyman MR and Wood PM 1983. Methane oxidation by Nitrosomonas europaea. Biochemical Journal 212, 31-37.
51. IPCC (Intergovernmental Panel on Climate Change) 2007. Climate Change 2007: The Physical Science Basis, Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Retrieved January 30, 2012 from http://ww.ipcc.ch/publicationsanddata.
52. Iwamoto M, Asanuma N and Hino T 1999. Effect of nitrate combined with fumarate on methanogenesis, fermentation, and cellulose digestion by mixed ruminal microbes in vitro. Animal Science Journal 70, 471-478.
53. Iwamoto M, Asanuma N and Hino T 2002. Ability of Selenomonas ruminantium, Veillonella parvula, and Wolinella succinogenes to reduce nitrate and nitrite with special reference to the suppression of ruminal methanogenesis. Anaerobe 8, 209-215.
54. Janssen PH and Kirs M 2008. Structure of the archaeal community of the rumen. Applied and Environmental Microbiology 74, 3619-3625.
55. Jarvis GN, Strompl C, Burgess DM, Skillman LC, Moore ERB and Joblin KN 2000. Isolation and identification of ruminal methanogens from grazing cattle. Current Microbiology 40, 327-332.
56. Jeyanathan J, Kirs M, Ronimus RS, Hoskin SO and Janssen PH 2011. Methanogen community structure in the rumens of farmed sheep, cattle and red deer fed different diets. FEMS Microbiology Ecology 76, 311-326.
57. Jiang QQ and Bakken LR 1999. Nitrous oxide production and methane oxidation by different ammonia-oxidizing bacteria. Applied and Environmental Microbiology 65, 2679-2684.
58. Kajikawa H, Valdes C, Hillman K, Wallace RJ and Newbold CJ 2003. Methane oxidation and its coupled electron-sink reactions in ruminal fluid. Letters in Applied Microbiology 36, 354-357.
59. Kaspar H 1982. Nitrite reduction to nitrous oxide by Propionibacteria: detoxication mechanism. Archives of Microbiology 133, 126-130.
60. Kaspar HF and Tiedje JM 1981. Dissimilatory reduction of nitrate and nitrite in the bovine rumen: nitrous oxide production and effect of acetylene. Applied and Environmental Microbiology 41, 705-709.
61. Kempton TJ, Murray RM and Leng RA 1976. Methane production and digestibility measurements in grey-Kangaroo and sheep. Australian Journal of Biological Sciences 29, 209-214.
62. Klieve AV, Ouwerkerk D and Maguire AJ 2012. Archaea in the foregut of macropod marsupials: PCR and amplicon sequence-based observations. Journal of Applied Microbiology 113, 1065-1075.
63. Klieve AV, Hennessy D, Ouwerkerk D, Forster RJ, Mackie RI and Attwood GT 2003. Establishing populations of Megasphaera elsdenii YE 34 and Butyrivibrio fibrisolvens YE 44 in the rumen of cattle fed high grain diets. Journal of Applied Microbiology 95, 621-630.
64. Knittel K, Losekann T, Boetius A, Kort R and Amann R 2005. Diversity and distribution of methanotrophic archaea at cold seeps. Applied and Environmental Microbiology 71, 467-479.
65. Krause DO, Bunch RJ, Conlan LL, Kennedy PM, Smith WJ, Mackie RI and McSweeney CS 2001. Repeated ruminal dosing of Ruminococcus spp. does not result in persistence, but changes in other microbial populations occur that can be measured with quantitative 16S-rRNA-based probes. Microbiology 147, 1719-1729.
66. Krehbiel CR, Rust SR, Zhang G and Gilliland SE 2003. Bacterial direct-fed microbials in ruminant diets: performance response and mode of action. Journal of Animal Science 81, 120-132.
67. Lee SS, Mantovani HC and Russell JB 2002a. The binding and degradation of nisin by mixed ruminal bacteria. FEMS Microbiology Ecology 42, 339-345.
68. Lee SS, Hsu JT, Mantovani HC and Russell JB 2002b. The effect of bovicin, HC5, a bacteriocin from Streptococcus bovis HC5, on ruminal methane production in vitro. FEMS Microbiology Letters 217, 51-55.
69. Leedle JAZ and Greening RC 1988. Postprandial changes in methanogenic and acidogenic bacteria in the rumens of steers fed high-forage or low-forage diets once daily. Applied and Environmental Microbiology 54, 502-506.
70. Lettat A, Noziere P, Berger C and Martin C 2012a. Method for reducing methane production in a ruminant animal. In World Intellectual Property Organization. Retrieved December 10, 2012, from http://www.sumobrain.com/ patents/wipo/wo2012147044.html
71. Lettat A, Noziere P, Silberberg M, Morgavi DP, Berger C and Martin C 2012b. Rumen microbial and fermentation characteristics are affected differently by bacterial probiotic supplementation during inuced lactic and subacute acidosis in sheep. BMC Microbiology 12, 142-154.
72. Li L, Davis J, Nolan J and Hegarty R 2012. An initial investigation on rumen fermentation pattern and methane emission of sheep offered diets containing urea or nitrate as the nitrogen source. Animal Production Science 52, 653-658.
73. Li M, Zhou M, Adamowicz E, Basarab JA and Guan LL 2011. Characterization of bovine ruminal epithelial bacterial communities using 16S rRNA sequencing, PCR-DGGE, and qRT-PCR analysis. Veterinary Microbiology 155, 72-80.
74. Lila ZA, Mohammed N, Yasui T, Kurokawa Y, Kanda S and Itabashi H 2004. Effects of a twin strain of Saccharomyces cerevisiae live cells on mixed ruminal microorizanism fermentation in vitro. Journal of Animal Science 82, 1847-1854.
75. Lopez S, McIntosh E, Wallace RJ and Newbold CJ 1999. Effect of adding acetogenic bacteria on methane production by mixed rumen microorganisms. Animal Feed Science and Technology 78, 1-9.
76. Lynch HA and Martin SA 2002. Effects of Saccharomyces cerevisiae culture and Saccharomyces cerevisiae live cells on in vitro mixed ruminal microorganism fermentation. Journal of Dairy Science 85, 2603-2608.
77. Macy JM, Ljungdahl LG and Gottschalk G 1978. Pathway of succinate and propionate formation in Bacteroides fragilis. Journal of Bacteriology 134, 84-91.
78. Martin C, Morgavi DP and Doreau M 2010. Methane mitigation in ruminants: from microbe to the farm scale. Animal 4, 351-365.
79. Mathieu F, Jouany JP, Senaud J, Bohatier J, Bertin G and Mercier M 1996. The effect of Saccharomyces cerevisiae and Aspergillus oryzae on fermentations in the rumen of faunated and defaunated sheep; protozoal and probiotic interactions. Reproduction Nutrition Development 36, 271-287.
80. McAllister TA, Beauchemin KA, Alazzeh AY, Baah J, Teather RM and Stanford K 2011. Review: the use of direct fed microbials to mitigate pathogens and enhance production in cattle. Canadian Journal of Animal Science 91, 193-211.
81. McGinn SM, Beauchemin KA, Coates T and Colombatto D 2004. Methane emissions from beef cattle: effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid. Journal of Animal Science 82, 3346-3356.
82. McKenney DJ, Shuttleworth KF, Vriesacker JR and Findlay WI 1982. Production and loss of nitric oxide from denitrification in anaerobic brookston clay. Applied and Environmental Microbiology 43, 534-541.
83. Miller TL and Wolin MJ 1985. Methanosphaera stadtmaniae gen. nov., sp. nov.: a species that forms methane by reducing methanol with hydrogen. Archives of Microbiology 141, 116-122.
84. Mitsumori M, Ajisaka N, Tajima K, Kajikawa H and Kurihara M 2002. Detection of Proteobacteria from the rumen by PCR using methanotroph-specific primers. Letters in Applied Microbiology 35, 251-255.
85. Morris MP, Cancel B and González-Más A 1958. Toxicity of nitrates and nitrites to dairy cattle. Journal of Dairy Science 41, 694-696.
86. Morvan B, RieuLesme F, Fonty G and Gouet P 1996. In vitro interactions between rumen H-2-producing cellulolytic microorganisms and H-2-utilizing acetogenic and sulfate-reducing bacteria. Anaerobe 2, 175-180.
87. Morvan B, Dore J, Rieulesme F, Foucat L, Fonty G and Gouet P 1994. Establishment of hydrogen-utilizing bacteria in the rumen of the newborn lamb. FEMS Microbiology Letters 117, 249-256.
88. Mutsvangwa T, Edwards IE, Topps JH and Paterson GFM 1992. The effect of dietary inclusion of yeast culture (Yea-Sacc) on patterns of rumen fermentation, food intake and growth of intensively fed bulls. Animal Production 55, 35-40.
89. Mwenya B, Santoso B, Sar C, Gamo Y, Kobayashi T, Arai I and Takahashi J 2004. Effects of including beta 1-4 galacto-oligosaccharides, lactic acid bacteria or yeast culture on methanogenesis as well as energy and nitrogen metabolism in sheep. Animal Feed Science and Technology 115, 313-326.
90. Nagaraja TG, Newbold CJ, Van Nevel CJ and Demeyer DI 1997. Manipulation of ruminal fermentation. In The rumen microbial ecosystem (ed. Hobson, PN and Stewart, CS), pp. 523-632. Chapman & Hall, London.
91. Newbold CJ, Wallace RJ and McIntoth FM 1996. Mode of action of the yeast Saccharomyces cerevisiae as a feed additive for ruminants. British Journal of Nutrition 76, 249-261.
92. Nollet L, Demeyer D and Verstraete W 1997. Effect of 2- bromoethanesulfonic acid and Peptostreptococcus productus ATCC 35244 addition on stimulation of reductive acetogenesis in the ruminal ecosystem by selective inhibition of methanogenesis. Applied and Environmental Microbiology 63, 194-200.
93. Nollet L, Mbanzamihigo L, Demeyer D and Verstraete W 1998. Effect of the addition of Peptostreptococcus productus ATCC 35244 on reductive acetogenesis in the ruminal ecosystem after inhibition of methanogenesis by cell-free supernatant of Lactobacillus plantarum 80. Animal Feed Science Technology 71, 49-66.
94. Paul K, Nonoh JO, Mikulski L and Brune A 2012. "Methanoplasmatales, " thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Applied Environmental Microbiology 78, 8245-8253.
95. Paul SS, Deb SM and Singh D 2011. Isolation and characterization of novel sulphate-reducing Fusobacterium sp. and their effects on in vitro methane emission and digestion of wheat straw by rumen fluid from Indian riverine buffaloes. Animal Feed Science and Technology 166, 132-140.
96. Perdok HB, Van Zijderveld SM, Newbold JR, Hulshof RBA, Deswysen D, Gerrits WJJ, Dijkstra J and Leng RA 2011. Compositions for reducing gastro-intestinal methanogenesis in ruminants. Retrieved October 10, 2012, from http://patentscope. wipo.int.
97. Pope PB, Smith W, Denman SE, Tringe SG, Barry K, Hugenholtz P, McSweeney CS, McHardy AC and Morrison M 2011. Isolation of Succinivibrionaceae implicated in low methane emissions from Tammar wallabies. Science 333, 646-648.
98. Raciti SM, Burgin AJ, Groffman PM, Lewis DN and Fahey TJ 2011. Denitrification in suburban lawn soils. Journal of Environmental Quality 40, 1932-1940.
99. Ragsdale SW and Pierce E 2008. Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochimica et Biophysica Acta-Proteins and Proteomics 1784, 1873-1898.
100. Rehberger TG and Hibberd CA 2000. Bacterial composition to reduce the toxic effects of high nitrate consumption in livestock. Patent USA, patent number 6, 120, 810. Oklahoma State University, USA.
101. Romero-Perez GA, Ominski KH, McAllister TA and Krause DO 2011. Effect of environmental factors and influence of rumen and hindgut biogeography on bacterial communities in steers. Applied and Environmental Microbiology 77, 258-268.
102. Russell JB and Wallace RJ 1997. Energy-yielding and energy-consuming reactions. In The rumen microbial ecosystem (ed. Hobson, PN and Stewart, CS), pp. 246-282. Blackie Academic and Professional, London.
103. Sadet-Bourgeteau S, Martin C and Morgavi DP 2010. Bacterial diversity dynamics in rumen epithelium of wethers fed forage and mixed concentrate forage diets. Veterinary Microbiology 146, 98-104.
104. Sakthivel PC, Kamra DN, Agarwal N and Chaudhry LC 2012. Effect of sodium nitrate and nitrate reducing bacteria in in vitro methane production and fermentation with buffalo rumen liquor. Asian-Australasian Journal of Animal Science 25, 812-817.
105. Sar C, Mwenya B, Pen B, Morikawa R, Takaura K, Kobayashi T and Takahashi J 2005a. Effect of nisin on ruminal methane production and nitrate/nitrite reduction in vitro. Australian Journal of Agricultural Research 56, 803-810.
106. Sar C, Mwenya B, Santoso B, Takaura K, Morikawa R, Isogai N, Asakura Y, Toride Y and Takahashi J 2005b. Effect of Escherichia coli wild type or its derivative with high nitrite reductase activity on in vitro ruminal methanogenesis and nitrate/nitrite reduction. Journal of Animal Science 83, 644-652.
107. Sar C, Mwenya B, Pen B, Takaura K, Morikawa R, Tsujimoto A, Kuwaki K, Isogai N, Shinzato I, Asakura Y, Toride Y and Takahashi J 2005c. Effect of ruminal administration of Escherichia coli wild type or a genetically modified strain with enhanced high nitrite reductase activity on methane emission and nitrate toxicity in nitrate-infused sheep. British Journal of Nutrition 94, 691-697.
108. Seo JK, Kim SW, Kim MH, Upadhaya SD, Kam DK and Ha JK 2010. Direct-fed microbials for ruminant animals. Asian-Australasian Journal of Animal Science 23, 1657-1667.
109. Simon J 2002. Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiology Reviews 26, 285-309.
110. Sprenger WW, van Belzen MC, Rosenberg J, Hackstein JH and Keltjens JT 2000. Methanomicrococcus blatticola gen. nov., sp. nov., a methanoland methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. International Journal of Systematic and Evolutionary Microbiology 50, 1989-1999.
111. St-Pierre B and Wright ADG 2012. Molecular analysis of methanogenic archaea in the forestomach of the alpaca (Vicugna pacos). BMC Microbiology 12, 1. http://www.biomedcentral.com/1471-2180/12/1
112. Steinfeld H, Gerber P, Wassenaar T, Castel V and Rosales M 2006. Livestock's long shadow: environmental issues and options. Food and Agriculture Organization of the United Nations: Rome. Retrieved January 30, 2012 http://www.fao. org/docrep/010/a0701e/a0701e00.htm
113. Sullivan HM and Martin SA 1999. Effects of a Saccharomyces cerevisiae culture on in vitro mixed ruminal microorganism fermentation. Journal of Dairy Science 82, 2011-2016.
114. Sundset MA, Edwards JE, Cheng YF, Senosiain RS, Fraile MN, Northwood KS, Praesteng KE, Glad T, Mathiesen SD and Wright AD 2009. Molecular diversity of the rumen microbiome of Norwegian reindeer on natural summer pasture. Microbial Ecology 57, 335-348.
115. Takahashi J and Young BA 1991. Prophylactic effect of l-cysteine on nitrate-induced alterations in respiratory exchange and metabolic rate in sheep. Animal Feed Science and Technology 35, 105-113.
116. Takahashi J, Ikeda M, Matsuoka S and Fujita H 1998. Prophylactic effect of L-cysteine to acute and subclinical nitrate toxicity in sheep. Animal Feed Science and Technology 74, 273-280.
117. Thauer RK, Jungermann K and Decker K 1977. Energy-conservation in chemotropic anaerobic bacteria. Bacteriological Reviews 41, 100-180.
118. Tiedje JM, Sexstone AJ, Myrold DD and Robinson JA 1982. Denitrification-ecological niches, competition and survival. Antonie Van Leeuwenhoek Journal of Microbiology 48, 569-583.
119. van Zijderveld SM, Gerrits WJJ, Dijkstra J, Newbold JR, Hulshof RBA and Perdok HB 2011. Persistency of methane mitigation by dietary nitrate supplementation in dairy cows. Journal of Dairy Science 94, 4028-4038.
120. van Zijderveld SM, Gerrits WJJ, Apajalahti JA, Newbold JR, Dijkstra J, Leng RA and Perdok HB 2010. Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. Journal of Dairy Science 93, 5856-5866.
121. Wallnofer P and Baldwin RL 1967. Pathway of propionate formation in Bacteroides ruminicola. Journal of Bacteriology 93, 504-505.
122. Whitford MF, Teather RM and Forster RJ 2001. Phylogenetic analysis of methanogens from the bovine rumen. BMC Microbiology 1, 5.
123. Wright AD, Toovey AF and Pimm CL 2006. Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveal more uncultured novel archaea. Anaerobe 12, 134-139.
124. Yoshii T, Asanuma N and Hino T 2003. Number of nitrate-and nitrite-reducing Selenomonas ruminantium in the rumen, and possible factors affecting its growth. Animal Science Journal 74, 483-491.