Interactions between microbial consortia in biofilms: A paradigm shift in rumen microbial ecology and enteric methane mitigation

Animal Production Science

Volumn 54, Issue 5, 2014, Pages 519-543

  Leng, R A ^a  

^a UNIVERSITY OF NEW ENGLAND   (Australia)

Author keywords

chlorinated hydrocarbons; direct interspecies electron transport; electron acceptors; formate; inter bacterial distance; motility symbiosis; partial pressure hydrogen; reductive acetogenesis; role of protozoa; short chain nitro compounds; syntrophism; transparent exopolymer particles; viscotactic spirochete

Indexed keywords

BACTERIUM; BIOFILM; BIOGENIC EMISSION; DIET; EMISSION CONTROL; ENZYME ACTIVITY; FERMENTATION; HYDROGEN; METHANE; METHANOGENESIS; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; MICROBIOLOGY; NITRATE; ORGANIC MATTER; PARADIGM SHIFT; PARTIAL PRESSURE; PROTOZOAN; RUMINANT;

EID: 84897505685     PISSN: 18360939     EISSN: 18365787     Source Type: Journal    
DOI: 10.1071/AN13381     Document Type: Article

References (177)

1. Abe M, Iriki T, Tobe N, Shibui H (1981) Sequestration of holotrich protozoa in the reticulo-rumen of cattle. Applied and Environmental Microbiology 41, 758-765.
2. Abecia L, Toral PG, Martín-García AI, Martínez G, Tomkins NW, Molina-Alcaide E, Newbold CJ, Yanez-Ruiz DR (2012) Effect of bromochloromethane on methane emission, rumen fermentation pattern, milk yield, and fatty acid profile in lactating dairy goats. Journal of Dairy Science 95, 2027-2036. doi:10.3168/jds.2011-4831
3. Alaboudi AR, 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. doi:10.4141/cjas85-099
4. Allison C, Macfarlane GT (1988) Effect of nitrate on methane production and fermentation by slunies of human faecal bacteria. Journal of General Microbiology 134, 1397-1405.
5. Anderson RC, Callaway TR, Van Kessel JA, Jung YS, Edrington TS, Nisbet DJ (2003) Effect of select nitrocompounds on ruminal fermentation, an initial look at their potential to reduce economic and environmental costs associated with ruminal methanogenesis. Bioresource Technology 90, 59-63. doi:10.1016/S0960- 8524(03)00086-5
6. Anderson RC, Carstens GE, Miller RK, Callaway TR, Schultz CL, Edrington TS, Harvey RB, Nisbet DJ (2006) Effect of oral nitroethane and 2 nitropropanol administration on methane-producing activity and volatile fatty acid production in the ovine rumen. Bioresource Technology 97, 2421-2426. doi:10.1016/j. biortech.2005.10.013
7. Anderson RC, Krueger NA, Stanton TB, Callaway TR, Edrington TS, Harvey RB, Jung YS, Nisbet DJ (2008) Effects of select nitrocompounds on in vitro ruminal fermentation during conditions of limiting or excess added reductant. Bioresource Technology 99, 8655-8661. doi:10.1016/j.biortech.2008.04.064
8. Anderson RC, Huwe JK, Smith DJ, Stanton TB, Krueger NA, Callaway TR, Edrington TS, Harvey RB, Nisbet DJ (2010) Effect of nitroethane, dimethyl-2-nitroglutarate and 2-nitro-methyl-propionate on ruminal methane production and hydrogen balance in vitro. Bioresource Technology 101, 5345-5349. doi:10.1016/j.biortech.2009.11.108
9. Annison EF, Lewis D (1959) 'Metabolism in the rumen.' (John Wiley and Sons: New York)
10. Asanuma N, Wamoto M, Hino T (1990) The production of formate, a substrate for methanogenesis, from compounds related with the glyoxalate cycle by mixed ruminal microbes. Journal of Animal Science 70, 67-73.
11. Asanuma N, Iwamoto M, Hino T (1998) Formate metabolism by ruminal microorganisms in relation to methanogenesis. Animal Science and Technology 69, 576-584.
12. Banerjee A (1994) 'Dairying systems in India. World animal review 79(2).' (FAO: Rome)
13. Bar-Zeev E, Berman-Frank I, Girshevitz O, Berman T (2012) Revised paradigm of aquatic biofilm formation facilitated by microgel transparent exopolymer particles. Proceedings of the National Academy of Sciences of the United States of America 109(23), 9119-9124. doi:10.1073/pnas.1203708109
14. Bath C, Morrison M, Ross EM, Hayes BJ, Cocks BG (2013) The symbiotic rumen microbiome and cattle performance: a brief review. Animal Production Science 53, 876-881.
15. Bauchop T (1967) Inhibition of rumen methanogens by methane analogues. Journal of Bacteriology 94, 171-175.
16. Bauchop T, Montfort D (1981) Cellulose fermentation by a rumen anaerobic fungus in both the absence and the presence of rumen methanogens. Applied and Environmental Microbiology 42, 1103-1110.
17. Beaty PS, McInerney MJ (1987) Growth of Syntrophomonas wolfei in pure cultures on crotonate. Archives of Microbiology 147, 389-393. doi:10.10 07/BF00406138
18. Bird SH, Hill MK, Leng RA (1979) The effects of defaunation of the rumen on the growth of lambs on low-protein-high-energy diets. The British Journal of Nutrition 42, 81-87. doi:10.1079/BJN1979 0091
19. Bird SH, Hegarty RS, Woodgate R (2008) Persistence of defaunation effects on digestion and methane production in ewes. Australian Journal of Experimental Agriculture 48, 152-155. doi:10.1071/EA07298
20. Bleicher K, Winter J (1994) Formate production and utilisation by methanogens and by sludge consortia: interference with the concept of interspecies formate transfer. Applied Microbiology and Biotechnology 40, 910-915. doi:10.1007/BF00173998
21. Boccazzi P, Patterson JA (2013) Isolation and initial characterization of acetogenic ruminal bacteria resistant to acidic conditions. Agricultural Food and Analytical Bacteriology 3, 129-144.
22. Bollinger RR, Barbas AS, Bush EL, Lin SS, ParkeraW(2007) Biofilms in the large bowel suggest an apparent function of the human vermiform appendix. Journal of Theoretical Biology 249, 826-831. doi:10.1016/j.jtbi.2007.08.032
23. Boone DR, Johnson RL, Liu Y (1989) Diffusion of the interspecies electron carriers H2 and formate in methanogenic ecosystems, and implications in the measurement of KM for H2 or formate uptake. Applied and Environmental Microbiology 55, 1735-1741.
24. Božic AK, Anderson RC, Carstens GE, Ricke SC, Callaway TR, Yokoyama MT, Wang JK, Nisbet D (2009) Effects of the methane-inhibitors nitrate, nitroethane, lauric acid, Lauricidin and the Hawaiian marine algae Chaetoceros on ruminal fermentation in vitro. Bioresource Technology 100, 4017-4025. doi:10.1016/j.biortech.2008.12.061
25. Breznak JA, Blum JS (1991) Mixotrophy in the termite gut acetogen, Sporomusa termitida. Archives of Microbiology 156, 105-110. doi:10.10 07/BF00290981
26. BrownEG,AndersonRC, CarstenscGC,Gutierrez-Banuelos H,McReynolds JL, Slay LJ, Callaway TR, Nisbet DJ (2011) Effects of oral nitroethane administration on enteric methane emissions and ruminal fermentation in cattle. Animal Feed Science and Technology 166-167, 275-281. doi:10.1016/j.anifeedsci.2011.04.017
27. Cheng K-J, Costerton JW (1980) The formation of microcolonies by rumen bacteria. Canadian Journal of Microbiology 26, 1104-1113. doi:10.11 39/m80-183
28. Cheng KJ, Fay JP, Howarth RE, Costerton JW (1980) Sequence of events in the digestion of fresh legume leaves by rumen bacteria. Applied and Environmental Microbiology 40, 613-625.
29. Cheng K-J, Fay JP, Coleman RN, Milligan LP, Costerton JW (1981) Formation of bacterial microcolonies on feed particles in the rumen. Applied and Environmental Microbiology 41, 298-305.
30. Cheng K-J, Phillippe RC, Majak W (1988) Identification of rumen bacteria that anaerobically degrade nitrate. Applied and Environmental Microbiology 34, 1099-1102.
31. Cheng K-J, McAllister TA, Costerton JW (1995) Biofilm of the ruminant digestive tract. In 'Microbial biofilms'. (Eds H Lappin-Scott, JM Costerton) pp. 221-232. (Cambridge University Press: Cambridge, UK)
32. Clarke RTJ (1977) Protozoa in the rumen ecosystem. In 'Microbial ecology of the gut'. (Eds RTJ Clarke, T Bauchop) pp. 251-275. (Academic Press: New York)
33. Coleman RN (1960) A sulphate-reducing bacterium from the sheep rumen. Journal of General Microbiology 22, 423-436. doi:10.1099/00221287-22-2-423
34. Cord-Ruwisch R, Seitz HJ, Conrad R (1988) The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor. Archives of Microbiology 149, 350-357. doi:10.1007/BF00411655
35. Costerton JW (2007) The biofilm primer 1. In 'Springer series on biofilms'. (Ed. C Eckey) p. 165. (Springer-Verlag: Berlin)
36. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JG, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annual Review of Microbiology 41, 435-464. doi:10.1146/annurev.mi.41.1001 87.002251
37. Cottle DJ, Nolan JV, Wiedemann SG (2011) Ruminant enteric methane mitigation: a review. Animal Production Science 51, 491-514. doi:10.10 71/AN10163
38. Crable BR, Plugge CML, McInerney MJ, Stams AJM (2011) Formate formation and formate conversion in biological fuels production. Enzyme Research 2011, 532536. doi:10.4061/2011/532536
39. Craig WM, Broderick GA, Ricker DB (1987) Quantitation of microorganisms associated with the particulate phase of ruminal ingesta. The Journal of Nutrition 117, 56-62.
40. Cungen L, Tingshuang SZG, Waldron S (1999) The 'Straw for Ruminants' project in China. Agricultural and natural resource economics discussion paper 4/99. School of Natural and Rural Systems Management, University of Queensland, Brisbane.
41. Czerkawski JW, Blaxter KL, Wainman FW (1966) The metabolism of oleic, linoleic and linolenic acids by sheep with reference to their effects on methane production. The British Journal of Nutrition 20, 349-362. doi:10.1079/ BJN19660035
42. Davey ME, O'Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews 64, 847-867. doi:10.1128/MMBR.64.4.847-867.2000
43. de Bok FAM, Plugge CM, Stams AJM (2004) Interspecies electron transfer in methanogenic propionate degrading consortia. Water Research 38, 1368-1375. doi:10.1016/j.watres.2003.11.028
44. Derwent R, Simmonds P, O'Doherty S, Manning A, Collins W, Stevenson D (2006) Global environmental impacts of the hydrogen economy. International Journal of Nuclear Hydrogen Production and Application 1, 57-67. doi:10.1504/IJNHPA.2006.009869
45. Devendra C, Leng RA (2011) Feed resources for animals in Asia: issues, strategies for use, intensification and integration for increased productivity. Asian-Australasian Journal of Animal Sciences 24, 303-321. doi:10.5713/ajas. 2011.r.05
46. Doetsch RN, Robinson RQ, Brown RE, Shaw JC (1953) Catabolic reactions of mixed suspensions of bovine rumen bacteria. Journal of Dairy Science 36, 825-831. doi:10.3168/jds.S0022-0302(53)91568-9
47. Dolberg F, Finlayson P (1995) Treated straw for beef production in China. World Animal Review 82, 14-21.
48. Dong X, Stams AJM (1995) Evidence for H2 and formate formation during syntrophic butyrate and propionate degradation. Anaerobe 1, 35-39. doi:10.1016/S1075-9964(95)80405-6
49. Dong X, Plugge CM, Stams AJM (1994) Anaerobic degradation of propionate by a mesophilic acetogenic bacterium in coculture and triculture with different methanogens. Applied and Environmental Microbiology 60, 2834-2838.
50. Dougherty RW (1968) Section 6. Physiology of eructation in ruminants. In 'Handbook of physiology. Volume V'. (Ed. CF Code) pp. 2695-2698. (American Physiological Society: Washington, DC)
51. Dwyer DF, Weeg-Aerssens E, Shelton DR, Tiedje JM (1988) Bioenergetic conditions of butyrate metabolism by a syntrophic, anaerobic bacterium in co-culture with hydrogen-oxidizing methanogenic and sulfidogenic bacteria. Applied and Environmental Microbiology 54, 1354-1359.
52. Eckard RJ, Grainger C, de Klein CAM (2010) Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livestock Science 130, 47-56. doi:10.1016/j.livsci.2010.02.010
53. Edwards JE, Huws SA, Kim EJ, Kingston-SmithAH(2007) Characterization of the dynamics of initial bacterial colonisation of non-conserved forage in the bovine rumen. FEMS Microbiology Ecology 62, 323-335. doi:10.1111/j.1574-6941. 2007.00392.x
54. Edwards JE, Huws SA, Kim EJ, Lee MRF, Kingston-Smith AH, Scollan ND (2008) Advances in microbial ecosystem concepts and their consequences for ruminant agriculture. Animal Production Science 2, 653-660.
55. Eugène M, Archimede H, SauvantD(2004) Quantitative meta-analysis on the effects of defaunation of the rumen on growth, intake and digestion in ruminants. Livestock Production Science 85, 81-97. doi:10.1016/S0301-6226(03) 00117-9
56. Farra PA, Satter LD (1971) Manipulation of the ruminal fermentation III. Effect of nitrate on ruminal volatile fatty acid production and milk composition. Journal of Dairy Science 54, 1018-1024. doi:10.3168/jds.S0022- 0302(71)85965-9
57. Felchner-Zwirello M, Winter J, Gallert J (2013) Interspecies distances between propionic acid degraders and methanogens in syntrophic consortia for optimal hydrogen transfer. Applied Microbiology and Biotechnology 97, 9193-9205. doi:10.1007/s00253-012-4616-9
58. Feng Y, Xu Y, Yu Y, Xie Z, Lin X (2012) Mechanisms of biochar decreasing methane emission from Chinese paddy soils. Journal of Soils Biology and Biochemistry 46, 80-88. doi:10.1016/j.soilbio.2011.11.016
59. Fonty G, Joblin K, Chavarot M, Roux R, Naylor G, Michallon F (2007) Establishment and development of ruminal hydrogenotrophs in methanogen free lambs. Applied and Environmental Microbiology 73, 6391-6403. doi:10.1128/AEM.00181-07
60. Forsberg CW, Lam K (1977) Use of adenosine-50-triphosphate as an indicator of the microbiota biomass in rumen contents. Applied and Environmental Microbiology 33, 528
61. GibsonGR (1990) Physiology and ecology of the sulphate-reducing bacteria. The Journal of Applied Bacteriology 69, 769-797. doi:10.1111/j.1365-2672.1990. tb01575.x
62. Goel G, Makkar HPS, Becker K (2009) Inhibition of methanogens by bromochloromethane: effects on microbial communities and rumen fermentation using batch and continuous fermentations. The British Journal of Nutrition 101, 1484-1492. doi:10.1017/S0007114508076198
63. Gordon GLR, Phillips MW (1998) The role of anaerobic gut fungi in ruminants. Nutrition Research Reviews 11, 133-168. doi:10.1079/NRR19980009
64. Greening RC, Leedle JA (1989) Enrichment and isolation of Acetitomaculum ruminis gen. nov., sp. nov.: acetogenic bacteria from the bovine rumen. Archives of Microbiology 151, 399-406. doi:10.1007/BF00416597
65. Gutierrez-Bañuelos H, Anderson RC, Carstens GE, Slay LJ, Ramlachan N, Horrocks SM, Callaway TR, Edrington TS, Nisbet DJ (2007) Zoonotic bacterial populations, gut fermentation characteristics and methane production in feedlot steers during oral nitroethane treatment and after the feeding of an experimental chlorate product. Anaerobe 13, 21-31. doi:10.1016/j.anaerobe.2006. 11.002
66. Hansen HH, Storm IMLD, SellAM(2012) Effect of biochar on in vitro rumen methane production. Acta Agriculturae Scandinavica. Section A-Animal Science 62, 305-309. doi:10.1080/09064702.2013.789548
67. Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiological Reviews 60, 439-471.
68. Hao TP, Do HQ, Preston TR, Leng RA (2009) Nitrate as a fermentable nitrogen supplement for goats fed forage based diets low in true protein. Livestock Research for Rural Development 21, Article #10. Available at http://www.lrrd.org/lrrd21/1/trin21010.htm. [Verified 11 February 2014]
69. Hegarty RS, Bird SH, Vanselow BA, Woodgate R (2008) Effects of the absence of protozoa from birth or from weaning on the growth and methane production of lambs. The British Journal of Nutrition 100, 1220-1227. doi:10.1017/S0007114508981435
70. Hook SE, Wright NDG, McBride BW (2010) Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010, 945785. doi:10.1155/2010/ 945785
71. Howard BH, Hungate RE (1976) Desulfovibrio of the sheep rumen. Applied and Environmental Microbiology 32, 592-602.
72. Hristov AN, Oh J, Firkins JL, Dijkstra J, Kebreab E, Waghorn G, Makkar HPS, Adesogan AT, Yang W, Lee C, Gerber PJ, Henderson B, Tricarico JM (2013) Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. Journal of Animal Science 91, 5045-5069. doi:10.2527/jas.2013-6583
73. HulshofRBA,Berndt A, Gerrits WJJ, Dijkstra J, van ZijderveldSM,Newbold JR, Perdok HB (2012) Dietary nitrate supplementation reduces methane emission in beef cattle fed sugarcane based diets. Journal of Animal Science 90, 2317-2323. doi:10.2527/jas.2011-4209
74. Hume ID (1982) 'Digestive physiology and nutrition of marsupials.' (Cambridge University Press: Cambridge, UK)
75. Hungate RE (1966) 'The rumen and its microbes.' (Academic Press: New York)
76. Hungate RE, Smith W, Bauchop T, Yu I, Rabinowitz JC (1970) Formate as an intermediate in the bovine rumen fermentation. Journal of Bacteriology 102, 389-397.
77. Huws SA, Mayorga OL, Theodorou MK, Onime LA, Kim EJ, Cookson AH, Newbold CJ, Kingston-Smith AH (2013) Successional colonization of perennial ryegrass by rumen bacteria. Letters in Applied Microbiology 56, 186-196. doi:10.1111/lam.12033
78. Immig I, Demeyer D, Fiedler D, Van Nevel C, Mbanzamihigo L (1996) Attempts to induce reductive acetogenesis into a sheep rumen. Archives of Animal Nutrition 49, 363-370.
79. Janssen PH (2010) Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Animal Feed Science and Technology 160, 1-22. doi:10.1016/j.anifeedsci.2010.07.002
80. Joblin KN (1999) Ruminal acetogens and their potential to lower ruminant methane emissions. Australian Journal of Agricultural Research 50, 1307-1313. doi:10.1071/AR99004
81. Johnson ED, Wood AS, Stone JB, Moran ET Jr (1972) Some effects of methane inhibition in ruminants (steers). Canadian Journal of Animal Science 52, 703-712. doi:10.4141/cjas72-083
82. Kajikawa H, Newbold CJ (2003) Methane oxidation in the rumen. Journal of Animal Science 78, 291
83. Kajikawa H, Valdes C, Hillman K, Wallace RJ, Newbold CJ (2003) Methane oxidation and its coupled electron-sink reactions in ruminal fluid. Letters in Applied Microbiology 36, 354-357. doi:10.1046/j.1472-765X.2003.01317.x
84. Kempton TJ, Murray RM, Leng RA (1976) Methane production and digestibility measurements in grey kangaroo and sheep. Australian Journal of Biological Sciences 29, 209-214.
85. Kim CC (2012) Identification of rumen methanogens, characterization of substrate requirements and measurement of hydrogen thresholds. MSc Thesis, Massey University, Palmerston North, New Zealand.
86. Klieve AV, Ouwerkerk D (2007) Comparative greenhouse gas emissions from herbivores. In '7th international symposium on the nutrition of herbivores'. (Eds QX Meng, LP Ren, ZJ Cao) pp. 487-500. (China Agricultural University Press: Beijing, China)
87. Knight T, Ronimus RS, Dey D, Tootill C, Naylor G, Evans P, Molano G, Smith A, Tavendale M, Pinares-Patino CS, Clark H (2011) Chloroform decreases rumen methanogenesis and methanogen populations without altering rumen function in cattle. Animal Feed Science and Technology 166-167, 101-112. doi:10.1016/j.anifeedsci.20 11.04.059
88. Krebs GL (1987) The rumen ecosystem-kinetics of microbial pools and effects on microbial protein yield. PhD Thesis, University of New England, Armidale, NSW.
89. Le Van TD, Robinson JA, Ralph J, Greening RC, Smolenski WJ, Leedle JAZ, Schaefer DM (1998) Assessment of reductive acetogenesis with indigenous ruminal bacterium populations and Acetitomaculum ruminis. Applied and Environmental Microbiology 64, 3429-3436.
90. Leedle JAZ, Greening RC (1988) Methanogenic and acidogenic bacteria in the bovine rumen: postprandial changes after feeding high-or lowforage diets once daily. Applied and Environmental Microbiology 54, 505-506.
91. Leng RA (1991) Improving ruminant production and reducing methane emissions from ruminants by strategic supplementation. A report prepared for the Environmental Protection Agency of the USA. EPA/400/1-91/004. Available at http://nepis.epa.gov/[Verified 3 August 2013]
92. Leng RA (2004) Requirements for protein meals for ruminant meat production in developing countries. In 'Protein sources for the animal feed industry. Expert consultation and workshop,Bangkok'. pp. 225-254.
93. (FAO: Rome) Available at http://www.fao.org/docrep/007/y5019e/y5019e0f. htm [Verified 18 February 2014]
94. Leng RA (2005) Metabolisable protein requirements of ruminants fed roughage based diets. In 'International AHAT/BSAT conference on livestock-crop systems to meet the challenges of globalisation. Vol. 1'. (Eds P Rawlinson, C Wachirapakorn, P Pakdee, M Wanapat) pp. 330-347. (British Society of Animal Science: Penicuik, UK)
95. Leng RA (2008) 'The potential of feeding nitrate to reduce enteric methane production in ruminants.' (Department of Climate Change, Commonwealth Government of Australia: Canberra) Available at http://www.penambulbooks.com [Verified 11 February 2014]
96. Leng RA (2011) The rumen- A fermentation vat or a series of organized structured microbial consortia: implications for the mitigation of enteric methane production by feed additives. Livestock Research for Rural Development 23, Article #258. Available at http://www.lrrd.org/lrrd23/12/leng23258.htm. [Verified 3 August 2013]
97. Leng RA, Inthapanya S, Preston TR (2012a) Biochar lowers net methane production from rumen fluid in vitro. Livestock Research for Rural Development 24, Article #103. Available at http://www.lrrd.org/lrrd24/6/sang24103.htm. [Verified 3 August 2013]
98. Leng RA, Preston TR, Inthapanya S (2012b) Biochar reduces enteric methane and improves growth and feed conversion in local 'Yellow' cattle fed cassava root chips and fresh cassava foliage. Livestock Research for Rural Development 24, Article #199. Available at http://www.lrrd.org/lrrd24/11/leng24199.htm. [Verified 3 August 2013]
99. Leng RA, Preston TR, Inthapanya S (2012c) Methane production is reduced in an in vitro incubation when the rumen fluid is taken from cattle that previously received biochar in their diet. Livestock Research for Rural Development 24, Article #211. Available at http://www.lrrd.org/lrrd24/11/ sang24211.htm. [Verified 3 August 2013]
100. Leng RA, Inthapanya S, Preston TR (2013) All biochars are not equal in lowering methane production in in vitro rumen incubations. Livestock Research for Rural Development 25, Article #106. Available at http://www.lrrd.org/lrrd25/ 6/leng25106.htm [Verified 9 August 2013]
101. LilaZA,MohammedN, TatsuokaN, KandaS, KurokawaY, ItabashiH(2004) Effect of cyclodextrin diallyl maleate on methane production, ruminal fermentation andmicrobes in vitro and in vivo. Animal Science Journal 75, 15-22. doi:10.1111/j.1740-0929.2004.00149.x
102. Liu YX, Yang M, Wu YM, Wang HL, Chen YX, Wu WX (2011) Reducing CH4 and CO2 emissions from water-logged paddy soil with biochar. Journal of Soils and Sediments 11, 930-939. doi:10.1007/s11368-011-0376-x
103. Liu F, Rotaru A-E, Shrestha PM, Malvankar NS, Nevin K, LovleyDR (2012) Promoting direct interspecies electron transfer with activated carbon. Energy and Environmental Science 5, 8982-8989. Available at http://works.bepress.com/ kelly-nevin/59 [Verified 3 August 2013]
104. Loughnan M (1982) Methane synthesis in the rumen in the presence and absence of chemical manipulators of fermentation. MRurSci Thesis, University of New England, Armidale, NSW.
105. Lovley DR (1985) Minimum threshold for hydrogen metabolism in methanogenic bacteria. Applied and Environmental Microbiology 49, 1530-1531.
106. Lovley D, Godwin S (1988) Hydrogen concentrations as an indicator of the predominant terminal electron-accepting reactions in aquatic sediments. Geochimica et Cosmochimica Acta 52, 2993-3003. doi:10.1016/0016-7037(88)90163-9
107. Lovley DR, Dwyer DF, Klug MJ (1982) Kinetic analysis of competition between sulfate reducers and methanogens for hydrogen in sediments. Applied and Environmental Microbiology 43, 1373-1379.
108. Lovley DR, Greening RC, Ferry JG (1984) Rapidly growing rumen methanogenic organism that synthesizes Coenzyme M and has a high affinity for formate. Applied and Environmental Microbiology 48, 81-87.
109. Lowe SE, Theodorou MK, Trinci APJ (1987) Cellulases and xylanase of an anaerobicrumenfungusgrown onwheat straw, wheat straw holocellulose, cellulose, and xylan. Applied and Environmental Microbiology 53, 1216-1223.
110. Madsen J, Bjerg BS, Hvelplund T, Weisbjerg MR, Lund P (2010) Methane and carbon dioxide ratio in excreted air for quantification of methane production in ruminants. Livestock Science 129, 223-227. doi:10.1016/j.livsci.2010.01.001
111. Malvankar NS, Lovley DR (2012) Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5, 1039-1046. doi:10.1002/cssc.201100733
112. Martínez Amador SY, Garza-García Y, Rodríguez de la Garza JA, Rodríguez Martínez J (2011) Nitrate reduction, sulfate reduction and methanogenesis interrelation in fixed and suspended bed batch reactors. Current Research Journal of Biological Sciences 3, 591-596.
113. Marty RJ, Demeyer DI (1973) The effect of inhibitors of methane production on fermentation pattem and stoichiometry in vitro using rumen contents from sheep given molasses. The British Journal of Nutrition 30, 369-376. doi:10.1079/BJN19730041
114. Mayorga OL, Huws SA, Kim EJ, Kingston-Smith AH, Newbold CJ, Theodorou MK (2007) Biofilm formation by rumen microbes on fresh perennial ryegrass under in vitro anaerobic conditions. In 'UK Molecular Microbial Ecology Group 13th Meeting, University of Liverpool, 16-17 July 2007'.
115. McAllister TA, Cheng KJ (1996) Microbial strategies in the ruminal digestion of cereal grains. Animal Feed Science and Technology 62, 29-36. doi:10.1016/S0377-8401(96)01003-6
116. McAllister TA, Newbold CJ (2008) Redirecting rumen fermentation to reduce methanogenesis. Australian Journal of Experimental Agriculture 48, 7-13. doi:10.1071/EA07218
117. McAllister TA, Bae HD, Jones GA, Cheng KJ (1994) Microbial attachment and feed digestion in the rumen. Journal of Animal Science 72, 3004-3018.
118. McCrabb GJ, Berger KT, Magner T, May C, Hunter RA (1997) Inhibiting methane production in Brahman cattle with a novel compound and the effects on growth. Australian Journal of Agricultural Research 48, 323-329. doi:10.1071/A96119
119. McInerney MJ, Bryant MP, Pfennig N (1979) Anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Archives of Microbiology 122, 129-135. doi:10.1007/BF00411351
120. McInerney MJ, Bryant MR, Hespell B, CostertonW(1981) Syntrophomonas wolfei gen. nov. sp. nov., an anaerobic, syntrophic, fatty acid oxidising bacterium. Applied and Environmental Microbiology 41, 1029-1039.
121. Michalowski T, Muszynski P (1978) Diurnal variations in number of ciliate protozoa in the rumen of sheep fed once and twice daily. The Journal of Agricultural Science 90, 1-5. doi:10.1017/S0021859600048528
122. Miller TL (1995) Ecology of methane production and hydrogen sinks in the rumen. In 'Ruminant physiology: digestion, metabolism, growth and reproduction'. (Eds W von Engelhardt, S Leonhard-Marek, G Breves, D Giesecke) pp. 317-331. (Ferdinand Enke Verlag: Stuttgart, Germany)
123. Miller TL, Wolin MJ (1973) Formation of hydrogen and formate by Ruminococcus albus. Journal of Bacteriology 116, 836-846.
124. Mitsumori M, Ajisaka N, Tajima K, Kajikawa H, Kurihara M (2002) Detection of Proteobacteria from the rumen by PCR using methanotroph-specific primers. Letters in Applied Microbiology 35, 251-255. doi:10.1046/j.1472-765X.2002.01172. x
125. Mitsumori M, Shinkai T, Takenaka A, Enishi O, Higuchi K, Kobayashi Y, Nonaka I, Asanuma N, Denman SE, McSweeney CS (2012) Responses in digestion, rumen fermentation and microbial populations to inhibition of methane formation by a halogenated methane analogue. The British Journal of Nutrition 108, 482-491. doi:10.1017/S000711 4511005794
126. Morgavi DP, Forano E, Martin C, Newbold CJ (2010) Microbial ecosystem and methanogenesis in ruminants. Animal Feed Science and Technology 4, 1024-1036.
127. Morita I, Malvankar NS, Franks AE, Summers ZM, Giloteaux L, Rotaru AE, Rotaru C, Lovley DR (2011) Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. MBio 2, e00159-11. doi:10.1128/mBio.00159-11
128. Mosoni P, Martin C, Forano E, Morgavi DP (2011) Long-term defaunation increases the abundance of cellulolytic ruminococci and methanogens but does not affect the bacterial and methanogen diversity in the rumen. Journal of Animal Science 89, 783-791. doi:10.2527/jas.2010-2947
129. Moura JG, Gonzales P, Moura I, Fauque G (2007) Dissimilatory nitrate and nitrite ammonification by sulphate-reducing eubacteria. In 'Sulphurreducing bacteria environmental and engineering systems'. (Eds LL Barton, WA Hamilton) pp. 241-264. (Cambridge University Press: Cambridge, UK)
130. Murphy MR, Drone PE, Woodford ST (1985) Factors stimulating migration of holotrich protozoa into the rumen. Applied and Environmental Microbiology 49, 1329-1331.
131. Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nature Reviews. Microbiology 6, 441-454.
132. Nagpal R, Puniya AK, Griffith GW, Goel G, Puniya M, Sehgal JP, Singh K (2009) Chapter 17. Anaerobic rumen fungi: potential and applications. In 'Agriculturally important micro-organisms. Vol. 1'. (Eds GG Khachatourians, DK Arora, TP Rajendran, AK Srivastava) pp. 375-393. (Academic World International: Kamal, India)
133. Nolan JV, Hegarty RS, Hegarty J, Godwin IR, Woodgate R (2010) Effects of dietary nitrate on rumen fermentation, methane production and digesta kinetics in sheep. Animal Production Science 50, 801-806. doi:10.1071/AN09211
134. Oremland RS (1988) Biochemistry of methanogenic bacteria. In 'Biology of anaerobic microorganisms'. (Ed. AJB Zehnder) pp. 641-705. (John Wiley & Sons: New York)
135. Orpin CG, Hail FJ (1983) Surface structures of the rumen holotrich protozoon Isotricha intestinalis with particular reference to the attachment zone. Current Microbiology 8, 321-325. doi:10.1007/BF01573702
136. Orpin CG, Letcher AJ (1978) Some factors controlling the attachment of the rumen holotrich protozoa Isotricha intestinalis and I. prostoma to plant particles in vitro. Journal of General Microbiology 106, 33-40. doi:10.1099/00221287-106-1-33
137. Ouwerkerk D, Maguire AJ, McMillen L, Klieve AV (2009) Hydrogen utilising bacteria from the forestomach of eastern grey (Macropus giganteus) and red (Macropus rufus) kangaroos. Animal Production Science 49, 1043-1051. doi:10.1071/EA08294
138. Pinder RS, Patterson JA (2012) Glucose and hydrogen utilization by an acetogenic bacterium isolated from ruminal contents. Agricultural Food and Analytical Bacteriology 2, 253-274.
139. Preston TR, Leng RA (1987) 'Matching livestock systems to available resources in the tropics and subtropics.' (Penambul Books: Armidale, NSW).
140. Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Annual Review of Microbiology 57, 369-394. doi:10.1146/annurev.micro.57.03 0502.090759
141. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435, 1098-1101. doi:10.1038/nature03661
142. Rodríguez CJ, González J, Alvir MR, Redondo R, Cajarville C (2003) Effects of feed intake on composition of sheep rumen contents and their microbial population size. The British Journal of Nutrition 89, 97-103. doi:10.1079/BJN2002752
143. Rowe JB, Loughnan ML, Nolan JV, Leng RA (1979) Secondary fermentation in the rumen of a sheep given a diet based on molasses. The British Journal of Nutrition 41, 393-397. doi:10.1079/BJN1979 0048
144. Sawyer MS, Hoover WJ, Sniffen CJ (1974) Effects of a ruminal methane inhibitor on growth and energy metabolism in the ovine. Journal of Animal Science 38, 908-914.
145. Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiology and Molecular Biology Reviews 61, 262-280.
146. Schink B, Thauer RK (1988) Energetics of syntrophic methane formation and the influence of aggregation. In 'Granular anaerobic sludge: microbiology and technology'. (Eds G Lettinga, AJB Zehnder, JTC Grotenhuis, LW Hulshoff-Pol) pp. 5-17. (Pudoc: Wageningen, The Netherlands)
147. Sharp WM, Johnson RR, Owens FN (1982) Ruminal VFA production with steers fed whole or ground corn grain. Journal of Animal Science 55, 1505-1514.
148. Shi Y, Weimer P, Ralph J (1997) Formation of formate and hydrogen, and flux of reducing equivalents and carbon in Ruminococcus flavefaciens FD-1. Antonie van Leeuwenhoek 72, 101-109. doi:10.1023/A:1000 256221938
149. Song H, Clarke WP, Blackall LL (2005) Concurrent microscopic observations and activity measurements of cellulose hydrolyzing and methanogenic populations during the batch anaerobic digestion of crystalline cellulose. Biotechnology and Bioengineering 91, 369-378. doi:10.1002/bit.20517
150. Sophal C, Khang DN, Preston TR, Leng RA (2013) Nitrate replacing urea as a fermentable N source decreases enteric methane production and increases the efficiency of feed utilization in Yellow cattle. Livestock Research for Rural Development 25, Article #113. http://www.lrrd.org/lrrd25/7/soph25113.htm [Verified 14 July 2013]
151. Sophea IV, Preston TR (2011) Effect of different levels of supplementary potassium nitrate replacing urea on growth rates and methane production in goats fed rice straw, mimosa foliage and water spinach. Livestock Research for Rural Development 23, Article #71. http://www.lrrd.org/lrrd23/4/soph23071.htm [Verified 5 August 2013]
152. Stams AJM, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nature Reviews. Microbiology 7, 568-577. doi:10.1038/nrmicro2166
153. Stanton TB, Canale-Parola E (1979) Enumeration and selective isolation of rumen spirochetes. Applied and Environmental Microbiology 38, 965-973.
154. Stanton TB, Canale-Parola E (1980) Treponema bryantii sp. nov. a rumen spirochete that interacts with cellulolytic bacteria. Archives of Microbiology 127, 145-156. doi:10.1007/BF00428018
155. Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, de Haan C (2006) 'Livestock's long shadow: environmental issues and options.' (Food and Agriculture Organisation: Rome).
156. Stewart PS (2003) Diffusion in biofilms. Journal of Bacteriology 185, 1485-1491. doi:10.1128/JB.185.5.1485-1491.2003
157. Stocks PK, McCleskey CS (1964) Morphology and physiology of Methanomonas methanooxidans. Journal of Bacteriology 88, 1071-1077.
158. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annual Review of Microbiology 56, 187-209. doi:10.1146/annurev.micro.56.012302.160705
159. Suen G, Weimer PJ, Stevenson D, Aylward FO, Boyum J, Deneke J, Drinkwater C, Ivanova NN, Mikhailova N, Chertkov O, Goodwin LA, Currie CR, Mead D, Brumm PJ (2011) The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS ONE 6, e18814. doi:10.1371/journal. pone.0018814
160. Thiele JH, Zeikus JG (1988) Control of interspecies electron flow during anaerobic digestion: significance of formate transfer versus hydrogen transfer during syntrophic methanogenesis in flocs. Applied and Environmental Microbiology 54, 20-29.
161. Thiele JH, Chartrain M, Zeikus JG (1988) Control of interspecies electron flow during anaerobic-digestion-role of floc formation in syntrophic methanogenesis. Applied and Environmental Microbiology 54, 10-19.
162. Tokura M, Ushida K, Miyazaki K, Kojima Y(1997) Methanogens associated with rumen ciliates. FEMS Microbiology Ecology 22, 137-143. doi:10.1111/j.1574- 6941.1997.tb00365.x
163. Tomkins NW, Colegate SM, Hunter RA (2009) A bromochloromethane formulation reduces enteric methanogenesis in cattle fed grainbased diets. Animal Production Science 49, 1053-1058. doi:10.1071/EA08223
164. UNEP (2011)'Near-term climate protection and clean air benefits: actions for controlling short-lived climate forcers.' (United Nations Environment Programme (UNEP): Nairobi, Kenya)Available at:http://www.unep.org/publications/ ebooks/SLCF/UNEP. [Verified 3 August 2013].
165. Ushida K, Jouany JP (1996) Methane production associated with rumen ciliated protozoa and its effect on protozoan activity. Letters in Applied Microbiology 23, 129-132. doi:10.1111/j.1472-765X.1996.tb00047.x
166. Valdez RE, Alvarez FJ, Ferreiro HM, Guerra F, Lopez J, Priego A, Blackburn TH, Leng RA, Preston TR (1977) Rumen function in cattle given sugar cane. Tropical Animal Production 2, 260-272.
167. van Zijderveld SM (2011) Dietary strategies to reduce methane emissions from ruminants. PhD Thesis, Wageningen University, The Netherlands.
168. van Zijderveld SM, Gerrits WJJ, Apajalahti JA, Newbold JR, Dijkstra J, Leng RA, 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. doi:10.3168/jds.2010-3281
169. van Zijderveld SM, Gerrits WJJ, Dijkstra J, Newbold JR, Hulshof RBA, Perdok HB (2011) Persistency of methane mitigation by dietary nitrate supplementation in dairy cows. Journal of Dairy Science 94, 4028-4038. doi:10.3168/jds.2011-4236
170. Wallace RJ, Joblin KN (1985) Proteolytic activity of a rumen anaerobic fungus. FEMS Microbiology Letters 29, 19-25. doi:10.1111/j.1574-6968.1985. tb00828.x
171. Wang ZW, Chen S (2009) Potential of biofilm-based biofuel production. Applied and Environmental Microbiology 83, 1-18.
172. Warner ACI(1965) Factors influencingnumbers and kinds of microorganisms in the rumen'Physiology of digestion in the ruminant'. (Eds RW Dougherty, RS Allen, W Burroughs, NL Jacobson, AD McGilliard) 346-359. (Butterworths: Washington, DC)
173. Weimer PJ, Russell JB, Muck RE (2009) Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. Bioresource Technology 100, 5323-5331. doi:10.10 16/j.biortech.2009.04. 075
174. West SA, Griffin AS, Gardner A, Diggle SP (2006) Social evolution theory for microbes. Nature Reviews. Microbiology 4, 597-607. doi:10.1038/nrmicro1461
175. Williams AG (1986) Rumen holotrich ciliate protozoa. Microbiological Reviews 50, 25-49.
176. Williams P (2007) Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology 153, 3923-3938. doi:10.1099/mic.0.2007/012856-0
177. Wolin MJ (1979) The rumen fermentation: a model for microbial interactions in anaerobic ecosystems. Advances in Microbial Ecology 3, 49-77.