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Genome sequencing of rumen bacteria and archaea and its application to methane mitigation strategies

Published online by Cambridge University Press:  06 June 2013

S. C. Leahy*
Affiliation:
AgResearch, Grasslands Research Centre, Palmerston North 4442, New Zealand New Zealand Agricultural Greenhouse Gas Research Centre, Palmerston North 4442, New Zealand
W. J. Kelly
Affiliation:
AgResearch, Grasslands Research Centre, Palmerston North 4442, New Zealand
R. S. Ronimus
Affiliation:
AgResearch, Grasslands Research Centre, Palmerston North 4442, New Zealand New Zealand Agricultural Greenhouse Gas Research Centre, Palmerston North 4442, New Zealand
N. Wedlock
Affiliation:
New Zealand Agricultural Greenhouse Gas Research Centre, Palmerston North 4442, New Zealand AgResearch, Hopkirk Research Institute, Palmerston North 4442, New Zealand
E. Altermann
Affiliation:
AgResearch, Grasslands Research Centre, Palmerston North 4442, New Zealand
G. T. Attwood
Affiliation:
AgResearch, Grasslands Research Centre, Palmerston North 4442, New Zealand New Zealand Agricultural Greenhouse Gas Research Centre, Palmerston North 4442, New Zealand
*
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Abstract

Ruminant-derived methane (CH4), a potent greenhouse gas, is a consequence of microbial fermentation in the digestive tract of livestock. Development of mitigation strategies to reduce CH4 emissions from farmed animals is currently the subject of both scientific and environmental interest. Methanogens are the sole producers of ruminant CH4, and therefore CH4 abatement strategies can either target the methanogens themselves or target the other members of the rumen microbial community that produce substrates necessary for methanogenesis. Understanding the relationship that methanogens have with other rumen microbes is crucial when considering CH4 mitigation strategies for ruminant livestock. Genome sequencing of rumen microbes is an important tool to improve our knowledge of the processes that underpin those relationships. Currently, several rumen bacterial and archaeal genome projects are either complete or underway. Genome sequencing is providing information directly applicable to CH4 mitigation strategies based on vaccine and small molecule inhibitor approaches. In addition, genome sequencing is contributing information relevant to other CH4 mitigation strategies. These include the selection and breeding of low CH4-emitting animals through the interpretation of large-scale DNA and RNA sequencing studies and the modification of other microbial groups within the rumen, thereby changing the dynamics of microbial fermentation.

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Copyright
Copyright © The Animal Consortium 2013 

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Footnotes

*

Contributed equally to this review.

References

Baar, C, Eppinger, M, Raddatz, G, Simon, J, Lanz, C, Klimmek, O, Nandakumar, R, Gross, R, Rosinus, A, Keller, H, Jagtap, P, Linke, B, Meyer, F, Lederer, H, Schuster, SC 2003. Complete genome sequence and analysis of Wolinella succinogenes. Proceedings of the National Academy of Science USA 100, 1169011695.Google Scholar
Berg Miller, ME, Yeoman, CJ, Chia, N, Tringe, SG, Angly, FE, Edwards, RA, Flint, HJ, Lamed, R, Bayer, EA, White, BA 2012. Phage–bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome. Environmental Microbiology 14, 207227.Google Scholar
Berg Miller, ME, 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. Diversity and strain specificity of plant cell wall degrading enzymes revealed by the draft genome of Ruminococcus flavefaciens FD-1. PLoS One 4, e6650.Google Scholar
Buddle, BM, Denis, M, Attwood, GT, Altermann, E, Janssen, PH, Ronimus, RS, Pinares-Patino, CS, Muetzel, S, Wedlock, N 2011. Strategies to reduce methane emissions from farmed ruminants grazing on pasture. The Veterinary Journal 188, 1117.Google Scholar
Bryant, MP 1959. Bacterial species of the rumen. Bacteriological Reviews 23, 125153.CrossRefGoogle ScholarPubMed
Bryant, MP 1965. Rumen methanogenic bacteria. In Physiology of digestion of the ruminant (ed. RW Dougherty, RS Allen, W Burroughs, NL Jaskson and AD McGillard). Butterworths Publishing Inc., Washington, DC.Google Scholar
Carberry, CA, Kenny, DA, Han, S, McCabe, SM, Waters, SM 2012. The effect of phenotypic residual feed intake and dietary forage content on the rumen microbial community of beef cattle. Applied and Environmental Microbiology 78, 49494958.Google Scholar
Chaucheyras-Durand, F, Masséglia, S, Fonty, G, 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, 79317937.CrossRefGoogle ScholarPubMed
Clark, H 2013. Nutrition and host effects on methanogenesis in the grazing ruminant. Animal 7 (suppl. 1), 4148.Google Scholar
Clauss, M, Hume, ID, Hummel, J 2010. Evolutionary adaptations of ruminants and their potential relevance for modern production systems. Animal 4, 979992.Google Scholar
Czerkawski, JW, Breckenridge, G 1975. New inhibitors of methane production by rumen micro-organisms. Experiments with animals and other practical possibilities. British Journal of Nutrition 34, 447457.CrossRefGoogle ScholarPubMed
Dodd, D, Moon, YH, Swaminathan, K, Mackie, RI, Cann, IK 2010. Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic bacteroidetes. The Journal of Biological Chemistry 285, 3026130273.CrossRefGoogle ScholarPubMed
Dormitzer, PR, Grandi, G, Rappuoli, R 2012. Structural vaccinology starts to deliver. Nature Reviews Microbiology 10, 807813.CrossRefGoogle ScholarPubMed
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, 63916403.Google Scholar
Forde, BM, Neville, BA, O'Donnell, MM, Riboulet-Bisson, E, Claesson, MJ, Coghlan, A, Ross, RP, O'Toole, PW 2011. Genome sequences and comparative genomics of two Lactobacillus ruminis strains from the bovine and human intestinal tracts. Microbial Cell Factories 10 (suppl. 1), S13.Google Scholar
Fouts, DE, Szpakowski, S, Purushe, J, Torralba, M, Waterman, RC, Macneil, MD, Alexander, LJ, Nelson, KE 2012. Next generation sequencing to define prokaryotic and fungal diversity in the bovine rumen. PLoS One 7 (11), e48289.Google Scholar
Gagen, EJ, Mosoni, P, Denman, SE, Al Jassim, R, McSweeney, CS, Forano, E 2012. Methanogen colonisation does not significantly alter acetogen diversity in lambs isolated 17 h after birth and raised aseptically. Microbial Ecology 64, 628640.Google Scholar
Gressley, TF, Hall, MB, Armentano, LE 2011. Productivity, digestion, and health responses to hindgut acidosis in ruminants. Journal of Animal Science 89, 11201130.Google Scholar
Guan, LL, Nkrumah, JD, Basarab, JA, Moore, SS 2008. Linkage of microbial ecology to phenotype: correlation of rumen microbial ecology to cattle's feed efficiency. FEMS Microbiology Letters 288, 8591.CrossRefGoogle ScholarPubMed
Hernandez-Sanabria, E, Goonewardene, LA, Wang, Z, Durunna, ON, Moore, SS, Guan, LL 2012. Impact of feed efficiency and diet on adaptive variations in the bacterial community in the rumen fluid of cattle. Applied and Environmental Microbiology 78, 12031214.Google Scholar
Henderson, G, Naylor, GE, Leahy, SC, Janssen, PH 2010. Presence of novel, potentially homoacetogenic bacteria in the rumen as determined by analysis of formyltetrahydrofolate synthetase sequences from ruminants. Applied and Environmental Microbiology 76, 20582066.CrossRefGoogle ScholarPubMed
Hess, M, Sczyrba, 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, 463467.CrossRefGoogle ScholarPubMed
Hong, SH, Kim, JS, Lee, SY, In, YH, Choi, SS, Rih, JK, Kim, CH, Jeong, H, Hur, CG, Kim, JJ 2004. The genome sequence of the capnophilic rumen bacterium Mannheimia succiniciproducens. Nature Biotechnology 22, 12751281.Google Scholar
Hook, SE, Wright, AG, McBride, BW 2010. Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010, 945785.Google Scholar
Hungate, RE 1967. Hydrogen as an intermediate in the rumen fermentation. Archives of Microbiology 59, 158164.Google Scholar
Hungate, RE, Smith, W, Bauchop, T, Yu, I, Rabinowitz, JC 1970. Formate as an intermediate in the rumen fermentation. Journal of Bacteriology 102, 384397.Google Scholar
Innes, EA, Bartley, PM, Rocchi, M, Benavidas-Silvan, J, Burrells, A, Hotchkiss, E, Chianini, F, Canton, G, Katzer, F 2011. Developing vaccines to control protozoan parasites in ruminants: dead or alive? Veterinary Parasitology 180, 155163.CrossRefGoogle ScholarPubMed
Janssen, PH, Kirs, M 2008. Structure of the archaeal community of the rumen. Applied and Environmental Microbiology 74, 36193625.Google Scholar
Johnson, DE, Wood, AS, Stone, JB, Moran, ET 1972. Some effects of methane inhibition in ruminants (steers). Canadian Journal of Animal Science 52, 703712.Google Scholar
Joblin, K 1999. Ruminal acetogens and their potential to lower ruminant methane emissions. Australian Journal of Agricultural Research 50, 13071313.Google Scholar
Kelly, WJ, Leahy, SC, Altermann, E, Yeoman, J, Dunne, JC, Kong, Z, Pacheco, DM, Li, D, Noel, SJ, Moon, CD, Cookson, AL, Attwood, GT 2010. The glycobiome of the rumen bacterium Butyrivibrio proteoclasticus B316(T) highlights adaptation to a polysaccharide-rich environment. PLoS One 5, e11942.Google Scholar
Kenters, N, Henderson, G, Jeyanathan, J, Kittelmann, S, Janssen, PH 2011. Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium. Journal of Microbiological Methods 84, 5260.Google Scholar
Kim, M, Morrison, M, Yu, Z 2011. Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiology Ecology 76, 4963.Google Scholar
Koike, S, Handa, Y, Goto, H, Sakai, K, Miyagawa, E, Matsui, H, Ito, S, Kobayashi, Y 2010. Molecular monitoring and isolation of previously uncultured bacterial strains from the sheep rumen. Applied and Environmental Microbiology 76, 18871894.Google Scholar
Leahy, SC, Kelly, WJ, Altermann, E, Ronimus, RS, Yeoman, CJ, Pacheco, DM, Li, D, Kong, Z, McTavish, S, Sang, C, Lambie, SC, Janssen, PH, Dey, D, Attwood, GT 2010. The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS One 5, e8926.Google Scholar
Lee, GH, Kumar, S, Lee, JH, Chang, DH, Kim, DS, Choi, SH, Rhee, MS, Lee, DW, Yoon, MH, Kim, BC 2012. Genome sequence of Oscillibacter ruminantium strain GH1, isolated from rumen of Korean native cattle. Journal of Bacteriology 194, 6362.Google Scholar
Lee, JH, Rhee, MS, Kumar, S, Lee, GH, Chang, DH, Kim, DS, Choi, SH, Lee, DW, Yoon, MH, Kim, BC 2013. Genome sequence of Methanobrevibacter sp. strain JH1, isolated from rumen of Korean native cattle. Genome Announcements 1, e00002-13.Google Scholar
Liu, Y, Whitman, WB 2008. Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Annals of the New York Academy of Sciences 1125, 171189.Google Scholar
Martin, C, Morgavi, DP, Doreau, M 2010. Methane mitigation in ruminants: from microbe to the farm scale. Animal 4, 351365.Google Scholar
Marx, H, Graf, AB, Tatto, NE, Thallinger, GG, Mattanovich, D, Sauer, M 2011. Genome sequence of the ruminal bacterium Megasphaera elsdenii. Journal of Bacteriology 193, 55785579.CrossRefGoogle ScholarPubMed
McAllister, TA, Newbold, CJ 2008. Redirecting rumen fermentation to reduce methanogenesis. Australian Journal of Experimental Agriculture 48, 713.Google Scholar
McCrabb, GJ, Berger, KT, Magner, T, May, C, Hunter, RA 1997. Inhibiting methane production in Brahman cattle by dietary supplementation with a novel compound and the effects on growth. Australian Journal of Agricultural Research 48, 323329.Google Scholar
McKinlay, JB, Laivenieks, M, Schindler, BD, McKinlay, AA, Siddaramappa, S, Challacombe, JF, Lowry, SR, Clum, A, Lapidus, AL, Burkhart, KB, Harkins, V, Vieille, C 2010. A genomic perspective on the potential of Actinobacillus succinogenes for industrial succinate production. BMC Genomics 11, 680.Google Scholar
McSweeney, C, Mackie, R 2012. Micro-organisms and ruminant digestion: state of knowledge, trends and future prospects. Commission of Genetic Resources for Food and Agriculture. Background study paper No. 61. Retrieved December 4, 2012, from http://www.fao.org/docrep/016/me992e/me992e.pdf.Google Scholar
Morgavi, DP, Kelly, WJ, Janssen, PH, Attwood, GT 2013. Rumen microbial (met)genomics and its application to ruminant production. Animal 7 (suppl. 1), 184201.Google Scholar
Nyonyo, T, Shinkai, T, Tajima, A, Mitsumori, M 2013. Effect of media composition, including gelling agents, on isolation of previously uncultured rumen bacteria. Letters in Applied Microbiology 56, 6370.CrossRefGoogle ScholarPubMed
Paul, K, Nonoh, JO, Mikulski, L, Brune, A 2012. “Methanoplasmatales,” thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Applied and Environmental Microbiology 78, 82458253.Google Scholar
Pinares-Patiño, CS, Ulyatt, MJ, Lassey, KR, Barry, TN, Holmes, CW 2003. Rumen function and digestion parameters associated with differences between sheep in methane emissions when fed chaffed lucerne hay. Journal of Agricultural Science 140, 205214.Google Scholar
Pinares-Patiño, CS, McEwan, JC, Dodds, KG, Cárdenas, EA, Hegarty, RS, Koolaard, JP, Clark, H 2011a. Repeatability of methane emissions from sheep. Animal Feed Science and Technology 166–167, 210218.CrossRefGoogle Scholar
Pinares-Patiño, CS, Ebrahimi, SH, McEwan, JC, Dodds, KG, Clark, H, Luo, D 2011b. Is rumen retention time implicated in sheep differences in methane emission? Proceedings of the New Zealand Society of Animal Production 71, 219222.Google Scholar
Pukall, R, Lapidus, A, Nolan, M, Copeland, A, Glavina Del Rio, T, Lucas, S, Chen, F, Tice, H, Cheng, JF, Chertkov, O, Bruce, D, Goodwin, L, Kuske, C, Brettin, T, Detter, JC, Han, C, Pitluck, S, Pati, A, Mavrommatis, K, Ivanova, N, Ovchinnikova, G, Chen, A, Palaniappan, K, Schneider, S, Rohde, M, Chain, P, D'haeseleer, P, Göker, M, Bristow, J, Eisen, JA, Markowitz, V, Kyrpides, NC, Klenk, HP, Hugenholtz, P 2009. Complete genome sequence of Slackia heliotrinireducens type strain (RHS 1T). Standards in Genomic Sciences 1, 234241.Google Scholar
Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, Coutinho PM, Henrissat B, Nelson KE North American Consortium for Rumen Bacteria 2010. Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microbial Ecology 60, 721729.Google Scholar
Rea, S, Bowman, JP, Popovski, S, Pimm, C, Wright, AD 2007. Methanobrevibacter millerae sp. nov. and Methanobrevibacter olleyae sp. nov., methanogens from the ovine and bovine rumen that can utilize formate for growth. International Journal of Systematic and Evolutionary Microbiology 57, 450456.Google Scholar
Rosewarne, CP, Cheung, JL, Smith, WJ, Evans, PN, Tomkins, NW, Denman, SE, Ó Cuív, P, Morrison, M 2012. Draft genome sequence of Treponema sp. strain JC4, a novel spirochete isolated from the bovine rumen. Journal of Bacteriology 194, 4130.Google Scholar
Sakai, S, Imachi, H, Sekiguchi, Y, Tseng, IC, Ohashi, A, Harada, H, Kamagata, Y 2009. Cultivation of methanogens under low-hydrogen conditions by using the coculture method. Applied and Environmental Microbiology 75, 48924896.CrossRefGoogle ScholarPubMed
Seo, JK, Seon-Woo, K, Kim, MH, Santi, D, Kam, DK, Jong, KH 2010. Direct-fed microbials for ruminant animals. Asian-Australasian Journal of Animal Sciences 12, 16571667.Google Scholar
Spring, S, Visser, M, Lu, M, Copeland, A, Lapidus, A, Lucas, S, Cheng, J, Han, C, Tapia, R, Goodwin, L, Pitluck, S, Ivanova, N, Land, M, Hauser, L, Larimer, F, Rohde, M, Göker, M, Detter, J, Kyrpides, N, Woyke, T, Schaap, P, Plugge, C, Muyzer, G, Kuever, J, Pereira, I, Parshina, S, Berner-Latmani, R, Stams, A, Klenk, H 2012. Complete genome sequence of the sulfate-reducing firmicute Desulfotomaculum ruminis type strain (DLT). Standards in Genomic Sciences 7, 304319.Google Scholar
St-Pierre, B, Wright, ADG 2013. Diversity of gut methanogen in herbivorous animals. Animal 7 (suppl. 1), 4956.Google Scholar
Suen, G, Weimer, PJ, Stevenson, DM, Aylward, FO, Boyum, J, Deneke, J, Drinkwater, C, Ivanova, NN, Mikhailova, N, Chertkov, O, Goodwin, LA, Currie, CR, Mead, D, Brumm, PJ 2011a. The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS One 6, e18814.Google Scholar
Suen, G, Stevenson, DM, Bruce, DC, Chertkov, O, Copeland, A, Cheng, JF, Detter, C, Detter, JC, Goodwin, LA, Han, CS, Hauser, LJ, Ivanova, NN, Kyrpides, NC, Land, ML, Lapidus, A, Lucas, S, Ovchinnikova, G, Pitluck, S, Tapia, R, Woyke, T, Boyum, J, Mead, D, Weimer, PJ 2011b. Complete genome of the cellulolytic ruminal bacterium Ruminococcus albus 7. Journal of Bacteriology 193, 55745575.Google Scholar
Thorpe, A 2009. Enteric fermentation and ruminant eructation: the role (and control?) of methane in the climate change debate. Climate Change 93, 407431.Google Scholar
Van Nevel, CJ, Demeyer, D 1995. Feed additives and other interventions for decreasing methane emissions. In Biotechnology in animal feeds and animal feeding (ed. J Wallace and A Chesson), pp. 329349. VCH Publishers, New York, NY, USA.Google Scholar
Wedlock, DN, Janssen, PH, Leahy, S, Shu, D, Buddle, BM 2013. Progress in the development of vaccines against rumen methanogens. Animal (suppl. s2), 244252.Google Scholar
Wright, ADG, Klieve, AV 2011. Does the complexity of the rumen microbial ecology preclude methane mitigation? Animal Feed Science and Technology 166–167, 248253.Google Scholar
Wright, ADG, Kennedy, P, O'Neill, CJ, Toovey, AF, Popovski, S, Rea, SM, Pimm, CL, Klein, L 2004. Reducing methane emissions in sheep by immunization against rumen methanogens. Vaccine 22, 39763985.Google Scholar
Zhou, M, Hernandez-Sanabria, E, Guan, LL 2009. Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Applied and Environmental Microbiology 75, 65246533.Google Scholar
Zhou, M, Hernandez-Sanabria, E, Guan, LL 2010. Characterization of variation in rumen methanogenic communities under different dietary and host feed efficiency conditions, as determined by PCR-denaturing gradient gel electrophoresis analysis. Applied and Environmental Microbiology 76, 37763786.Google Scholar
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