The ruminal microbiome associated with methane emissions from ruminant livestock

Tapio, Ilma; Snelling, Timothy J.; Strozzi, Francesco; Wallace, R. John

doi:10.1186/s40104-017-0141-0

Cited by 391Ruminant Nutrition and Digestive PhysiologyAnaerobic Digestion and Biogas ProductionGut microbiota and health

The ruminal microbiome associated with methane emissions from ruminant livestock

Open access

Tapio, Ilma, Snelling, Timothy J., Strozzi, Francesco, Wallace, R. John·2017·Journal of Animal Science and Biotechnology

DOI 10.1186/s40104-017-0141-0PMC PMC5244708

Open this paper in CoChat — free account Open PDF

Abstract

Methane emissions from ruminant livestock contribute significantly to the large environmental footprint of agriculture. The rumen is the principal source of methane, and certain features of the microbiome are associated with low/high methane phenotypes. Despite their primary role in methanogenesis, the abundance of archaea has only a weak correlation with methane emissions from individual animals. The composition of the archaeal community appears to have a stronger effect, with animals harbouring the Methanobrevibacter gottschalkii clade tending to be associated with greater methane emissions. Ciliate protozoa produce abundant H 2 , the main substrate for methanogenesis in the rumen, and their removal (defaunation) results in an average 11% lower methane emissions in vivo, but the results are not consistent . Different protozoal genera seem to result in greater methane emissions, though community types (A, AB, B and O) did not differ. Within the bacteria, three different ‘ruminotypes’ have been identified, two of which predispose animals to have lower methane emissions. The two low-methane ruminotypes are generally characterized by less abundant H 2 -producing bacteria. A lower abundance of Proteobacteria and differences in certain Bacteroidetes and anaerobic fungi seem to be associated with high methane emissions. Rumen anaerobic fungi produce abundant H 2 and formate, and their abundance generally corresponds to the level of methane emissions. Thus, microbiome analysis is consistent with known pathways for H 2 production and methanogenesis, but not yet in a predictive manner. The production and utilisation of formate by the ruminal microbiota is poorly understood and may be a source of variability between animals.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1186/s40104-017-0141-0

Cites

112 of 112 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Methane is produced primarily via the hydrogenotrophic pathway as a result of the reduction of CO2, and less so through methylotrophic or acetoclastic pathways.
“Methane is produced primarily via the hydrogenotrophic pathway (Figure 1) as a result of the reduction of CO2, and less so through the utilization of methyl groups (methylotrophic pathway), or even less commonly from acetate (acetoclastic pathway; Morgavi et al., 2010; Tapio et al., 2017).”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Tapio et al., 2017
There is increased evidence that host genetics has an influential role on the microbial population residing in the rumen.
“Whilst there is increased evidence that host genetics has an influential role on the microbial population residing in the rumen (Tapio et al., 2017),”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Tapio et al., 2017
The ratio of bacteria:archaea reflects methane output from the animal, with positive correlations reported in a few studies, but results are not consistent.
“It has been suggested also that the ratio of bacteria:archaea reflects methane output from the animal with positive correlations reported in a few studies (Wallace et al., 2014; Auffret et al., 2017b), but results are not consistent (Tapio et al., 2017).”
From Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future (2018) · cites this paper as Tapio et al., 2017

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · see citing works
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0
Tamura, K., Dudley, J. T., Nei, M., & Kumar, S. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm092 · Cited by 28,734 · see citing works
Untitled work
(2014) · doi:10.59327/ipcc/ar5-9789291691432 · Cited by 5,217 · see citing works
<i>Faecalibacterium prausnitzii</i> is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J.-J., Blugeon, S., Bridonneau, C., Furet, J.-P., Corthier, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804812105 · Cited by 4,413 · see citing works
The Rumen and Its Microbes
Hungate, R. E. (2013) · Elsevier eBooks · doi:10.1016/c2013-0-12555-x · Cited by 3,060 · see citing works
Methane emissions from cattle
Johnson, K. A., & Johnson, D. E. (1995) · Journal of Animal Science · doi:10.2527/1995.7382483x · Cited by 2,714 · cited 1× · see citing works
“Ruminal CH4 production also represents a loss of energy (from 2 to 12% of gross energy intake [4]), which could in principle otherwise be available for animal growth or milk production.”
Background
Methanogenic archaea: ecologically relevant differences in energy conservation
Thauer, R. K., Kaster, A.-K., Seedorf, H., Buckel, W., & Hedderich, R. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1931 · Cited by 2,184 · see citing works
Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range
Henderson, G., Cox, F., Ganesh, S., Jonker, A., Young, W., Collaborators, G. R. C., Abecia, L., Angarita, E., Aravena, P., Nora Arenas, G., et al. (2015) · Scientific Reports · doi:10.1038/srep14567 · Cited by 1,682 · see citing works
Self-citation
Improved extraction of PCR-quality community DNA from digesta and fecal samples
Yu, Z., & Morrison, M. D. (2004) · BioTechniques · doi:10.2144/04365st04 · Cited by 1,668 · see citing works
Nutritional management for enteric methane abatement: a review
Beauchemin, K. A., Kreuzer, M., O’Mara, F. P., & McAllister, T. A. (2008) · Australian Journal of Experimental Agriculture · doi:10.1071/ea07199 · Cited by 1,162 · see citing works
Invited review: enteric methane in dairy cattle production: quantifying the opportunities and impact of reducing emissions
Knapp, J. R., Laur, G. L., Vadas, P. A., Weiss, W. P., & Tricarico, J. M. (2014) · Journal of Dairy Science · doi:10.3168/jds.2013-7234 · Cited by 1,002 · see citing works
Digestion and metabolism in the ruminant
Ziołecki, A. (1976) · Livestock Production Science · doi:10.1016/0301-6226(76)90025-7 · Cited by 999 · see citing works
Methane mitigation in ruminants: from microbe to the farm scale
Martin, C., Morgavi, D. P., & Doreau, M. (2009) · animal · doi:10.1017/s1751731109990620 · Cited by 887 · see citing works
Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics
Janssen, P. H. (2010) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2010.07.002 · Cited by 848 · see citing works
Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants.
Shabat, S. K. B., Sasson, G., Doron-Faigenboim, A., Durman, T., Yaacoby, S., Berg Miller, M. E., White, B. A., Shterzer, N., & Mizrahi, I. (2016) · The ISME Journal · doi:10.1038/ismej.2016.62 · Cited by 823 · see citing works
The rumen bacteria
Stewart, C. S., Flint, H. J., & Bryant, M. P. (1997) · The Rumen Microbial Ecosystem · doi:10.1007/978-94-009-1453-7_2 · Cited by 772 · see citing works
Microbial ecosystem and methanogenesis in ruminants
Morgavi, D. P., Forano, E., Martin, C., & Newbold, C. J. (2010) · animal · doi:10.1017/s1751731110000546 · Cited by 694 · see citing works
The Rumen Protozoa
Williams, A. G., & Coleman, G. S. (1991) · Cited by 675 · see citing works
Structure of the Archaeal Community of the Rumen
Janssen, P. H., & Kirs, M. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02812-07 · Cited by 655 · see citing works
The role of ciliate protozoa in the rumen
Newbold, C. J., de la Fuente, G., Belanche, A., Ramos-Morales, E., & McEwan, N. R. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01313 · Cited by 637 · see citing works
Relationships of feedlot feed efficiency, performance, and feeding behavior with metabolic rate, methane production, and energy partitioning in beef cattle1
Nkrumah, J. D., Okine, E. K., Mathison, G. W., Schmid, K., Li, C., Basarab, J. A., Price, M. A., Wang, Z., & Moore, S. S. (2006) · Journal of Animal Science · doi:10.2527/2006.841145x · Cited by 578 · see citing works
An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production
Hristov, A. N., Oh, J., Giallongo, F., Frederick, T. W., Harper, M. T., Weeks, H. L., Branco, A. F., Moate, P. J., Deighton, M. H., Williams, S. R. O., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1504124112 · Cited by 496 · see citing works
Cattle selected for lower residual feed intake have reduced daily methane production1,2
Hegarty, R. S., Goopy, J. P., Herd, R. M., & McCorkell, B. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-236 · Cited by 449 · see citing works
Microbe-microbe interactions
Wolin, M. J., Miller, T. L., & Stewart, C. S. (1997) · The Rumen Microbial Ecosystem · doi:10.1007/978-94-009-1453-7_11 · Cited by 425 · see citing works
Studies on the Rumen Flagellate Neocallimastix frontalis
Orpin, C. G. (1975) · Journal of General Microbiology · doi:10.1099/00221287-91-2-249 · Cited by 417 · see citing works
The rumen microbial metagenome associated with high methane production in cattle
Wallace, R. J., Rooke, J. A., McKain, N., Duthie, C.-A., Hyslop, J. J., Ross, D. W., Waterhouse, A., Watson, M., & Roehe, R. (2015) · BMC Genomics · doi:10.1186/s12864-015-2032-0 · Cited by 416 · see citing works
Self-citation
Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome
Shi, W., Moon, C. D., Leahy, S. C., Kang, D., Froula, J., Kittelmann, S., Fan, C., Deutsch, S., Gagic, D., Seedorf, H., et al. (2014) · Genome Research · doi:10.1101/gr.168245.113 · Cited by 414 · see citing works
Rumen Microbiome from Steers Differing in Feed Efficiency
Myer, P. R., Smith, T. P. L., Wells, J. E., Kuehn, L. A., & Freetly, H. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129174 · Cited by 406 · see citing works
Simultaneous Amplicon Sequencing to Explore Co-Occurrence Patterns of Bacterial, Archaeal and Eukaryotic Microorganisms in Rumen Microbial Communities
Kittelmann, S., Seedorf, H., Walters, W. A., Clemente, J. C., Knight, R. D., Gordon, J. I., & Janssen, P. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0047879 · Cited by 384 · see citing works
Anaerobic fungi (phylum Neocallimastigomycota ): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential
Gruninger, R. J., Puniya, A. K., Callaghan, T. M., Edwards, J. E., Youssef, N. H., Dagar, S. S., Fliegerova, K. O., Griffith, G. W., Forster, R. J., Tsang, A., et al. (2014) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12383 · Cited by 364 · see citing works
Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen
Poulsen, M., Schwab, C., Borg Jensen, B., Engberg, R. M., Spang, A., Canibe, N., Højberg, O., Milinovich, G., Fragner, L., Schleper, C., et al. (2013) · Nature Communications · doi:10.1038/ncomms2432 · Cited by 361 · see citing works
Bovine Host Genetic Variation Influences Rumen Microbial Methane Production with Best Selection Criterion for Low Methane Emitting and Efficiently Feed Converting Hosts Based on Metagenomic Gene Abundance
Roehe, R., Dewhurst, R. J., Duthie, C.-A., Rooke, J. A., McKain, N., Ross, D. W., Hyslop, J. J., Waterhouse, A., Freeman, T. C., Watson, M., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005846 · Cited by 359 · see citing works
Effect of DNA extraction methods and sampling techniques on the apparent structure of cow and sheep rumen microbial communities
Henderson, G., Cox, F., Kittelmann, S., Miri, V. H., Zethof, M., Noel, S. J., Waghorn, G. C., & Janssen, P. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074787 · Cited by 328 · see citing works
The Genome Sequence of the Rumen Methanogen Methanobrevibacter ruminantium Reveals New Possibilities for Controlling Ruminant Methane Emissions
Leahy, S. C., Kelly, W. J., Altermann, E., Ronimus, R. S., Yeoman, C. J., Pacheco, D. M., Li, D., Kong, Z., McTavish, S. M., Sang, C., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008926 · Cited by 318 · see citing works
Effect of Phenotypic Residual Feed Intake and Dietary Forage Content on the Rumen Microbial Community of Beef Cattle
Carberry, C. A., Kenny, D. A., Han, S., McCabe, M. S., & Waters, S. M. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.07759-11 · Cited by 311 · see citing works
Cellulose Fermentation by a Rumen Anaerobic Fungus in Both the Absence and the Presence of Rumen Methanogens
Bauchop, T., & Mountfort, D. O. (1981) · Applied and Environmental Microbiology · doi:10.1128/aem.42.6.1103-1110.1981 · Cited by 305 · see citing works
The Rumen Protozoa
Williams, A. G., & Coleman, G. S. (1992) · Brock/Springer series in contemporary bioscience · doi:10.1007/978-1-4612-2776-2 · Cited by 304 · see citing works
Mitigation of greenhouse gas emissions in livestock production - A review of technical options for non-CO2 emissions
Hristov, A. N., Oh, J.-A., Lee, C., Meinen, R. J., Montes, F., OTT, T. L., Firkins, J. L., Rotz, A. C., Dell, C. J., Adesogan, C., et al. (2013) · Socio-Environmental Systems Modeling · Cited by 303 · see citing works
The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro
Newbold, C. J., Lassalas, B., & Jouany, J. P. (1995) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.1995.tb01048.x · Cited by 296 · see citing works
Association of methanogenic bacteria with rumen ciliates
Vogels, G. D., Hoppe, W. F., & Stumm, C. K. (1980) · Applied and Environmental Microbiology · doi:10.1128/aem.40.3.608-612.1980 · Cited by 284 · see citing works
Two different bacterial community types are linked with the low-methane emission trait in sheep.
Kittelmann, S., Pinares-Patiño, C. S., Seedorf, H., Kirk, M. R., Ganesh, S., McEwan, J. C., & Janssen, P. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103171 · Cited by 277 · see citing works
Rates of production of methane in the rumen and large intestine of sheep
Murray, R. M., Bryant, A. M., & Leng, R. A. (1976) · British Journal Of Nutrition · doi:10.1079/bjn19760053 · Cited by 269 · see citing works
Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents
Weimer, P. J., Stevenson, D. M., Mantovani, H. C., & Man, S. L. C. (2010) · Journal of Dairy Science · doi:10.3168/jds.2010-3500 · Cited by 267 · see citing works
Genetic parameters for predicted methane production and potential for reducing enteric emissions through genomic selection
de Haas, Y., WINDIG, J. J., Calus, M. P. L., Dijkstra, J., de Haan, M., Bannink, A., & Veerkamp, R. F. (2011) · Journal of Dairy Science · doi:10.3168/jds.2011-4439 · Cited by 242 · see citing works
Heritability estimates of methane emissions from sheep
Pinares-Patiño, C. S., Hickey, S. M., Young, E. A., Dodds, K. G., MacLean, S., Molano, G., Sandoval, E., Kjestrup, H., Harland, R., Hunt, C., et al. (2013) · animal · doi:10.1017/s1751731113000864 · Cited by 228 · see citing works
Isolation of Succinivibrionaceae Implicated in Low Methane Emissions from Tammar Wallabies
Pope, P. B., Smith, W. J. M., Denman, S. E., Tringe, S. G., Barry, K., Hugenholtz, P., McSweeney, C. S., McHardy, A. C., & Morrison, M. (2011) · Science · doi:10.1126/science.1205760 · Cited by 225 · see citing works
Formate as an Intermediate in the Bovine Rumen Fermentation
Hungate, R. E., Smith, W. W., Bauchop, T., Yu, I. K., & Rabinowitz, J. C. (1970) · Journal of Bacteriology · doi:10.1128/jb.102.2.389-397.1970 · Cited by 225 · see citing works
Reducing methane emissions in sheep by immunization against rumen methanogens
WRIGHT, A. (2004) · Vaccine · doi:10.1016/j.vaccine.2004.03.053 · Cited by 176 · see citing works
Taxon-specific associations between protozoal and methanogen populations in the rumen and a model rumen system
Sharp, R., Ziemer, C. J., Stern, M. D., & Stahl, D. A. (1998) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.1998.tb01563.x · Cited by 176 · see citing works
Determining the culturability of the rumen bacterial microbiome
Creevey, C. J., Kelly, W. J., Henderson, G., & Leahy, S. C. (2014) · Microbial Biotechnology · doi:10.1111/1751-7915.12141 · Cited by 173 · see citing works
Rumen protozoa and methanogenesis: not a simple cause–effect relationship
Morgavi, D. P., Martin, C., Jouany, J. P., & Ranilla, M. J. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511002935 · Cited by 163 · see citing works
Effects of 3-nitrooxypropanol on methane emission, digestion, and energy and nitrogen balance of lactating dairy cows
Reynolds, C. K., Humphries, D. J., Kirton, P., Kindermann, M., Duval, S. M., & Steinberg, C. E. W. (2014) · Journal of Dairy Science · doi:10.3168/jds.2013-7397 · Cited by 159 · see citing works
New aspects and strategies for methane mitigation from ruminants
Kumar, S., Choudhury, P. K., Carro, M. D., Griffith, G. W., Dagar, S. S., Puniya, M., Calabro, S., Ravella, S. R., Dhewa, T., Upadhyay, R. C., et al. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-5365-0 · Cited by 152 · see citing works
Influence of rumen protozoa on methane emission in ruminants: a meta-analysis approach
Guyader, J., Eugène, M., Nozière, P., Morgavi, D. P., Doreau, M., & Martin, C. (2014) · animal · doi:10.1017/s1751731114001852 · Cited by 151 · see citing works
A Vaccine against Rumen Methanogens Can Alter the Composition of Archaeal Populations
Williams, Y. J., Popovski, S., Rea, S. M., Skillman, L. C., Toovey, A. F., Northwood, K. S., & Wright, A. G. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02453-08 · Cited by 151 · see citing works
Association of methanogenic bacteria with ovine rumen ciliates
Stumm, C. K., Gijzen, H. J., & Vogels, G. D. (1982) · British Journal Of Nutrition · doi:10.1079/bjn19820013 · Cited by 150 · see citing works
Study of methanogen communities associated with different rumen protozoal populations
Belanche, A., de la Fuente, G., & Newbold, C. J. (2014) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12423 · Cited by 147 · see citing works
The players may change but the game remains: network analyses of ruminal microbiomes suggest taxonomic differences mask functional similarity
Taxis, T. M., Wolff, S., Gregg, S. J., Minton, N. O., Zhang, C., Dai, J., Schnabel, R. D., Taylor, J. F., Kerley, M. S., Pires, J. C., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv973 · Cited by 146 · see citing works
Inter-Relationships between Certain Rumen Ciliate Protozoa
Eadie, J. M. (1962) · Journal of General Microbiology · doi:10.1099/00221287-29-4-579 · Cited by 146 · see citing works
Effects of ethyl-3-nitrooxy propionate and 3-nitrooxypropanol on ruminal fermentation, microbial abundance, and methane emissions in sheep
Martı́nez, G., Abecia, L., Arco, A., Cantalapiedra-Hijar, G., Martín-García, A. I., Molina‐Alcaide, E., Kindermann, M., Duval, S. M., & Yáñez-Ruíz, D. R. (2014) · Journal of Dairy Science · doi:10.3168/jds.2013-7398 · Cited by 140 · see citing works
The anaerobic fungi in rumen fibre digestion
Bauchop, T. (1981) · Agriculture and Environment · doi:10.1016/0304-1131(81)90021-7 · Cited by 139 · see citing works
Metagenomic Predictions: From Microbiome to Complex Health and Environmental Phenotypes in Humans and Cattle
Ross, E. M., Moate, P. J., Marett, L. C., Cocks, B., & Hayes, B. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073056 · Cited by 138 · see citing works
Conversion of choline methyl groups through trimethylamine into methane in the rumen
Neill, A., Grime, D. W., & DAWSON, R. M. C. (1978) · Biochemical Journal · doi:10.1042/bj1700529 · Cited by 130 · see citing works
Influence of hydrogen-consuming bacteria on cellulose degradation by anaerobic fungi
Marvin-Sikkema, F. D., Richardson, A. J., Stewart, C. S., Gottschal, J. C., & Prins, R. A. (1990) · Applied and Environmental Microbiology · doi:10.1128/aem.56.12.3793-3797.1990 · Cited by 129 · see citing works
Metagenomic analysis of the rumen microbial community following inhibition of methane formation by a halogenated methane analog
Denman, S. E., Martı́nez, G., Shinkai, T., Mitsumori, M., & McSweeney, C. S. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.01087 · Cited by 129 · see citing works
High-grain feeding causes strong shifts in ruminal epithelial bacterial community and expression of Toll-like receptor genes in goats
Liu, J., Bian, G., Zhu, W., & Mao, S. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00167 · Cited by 128 · see citing works
Links between methane flux and transcriptional activities of methanogens and methane oxidizers in a blanket peat bog
Freitag, T. E., Toet, S., Ineson, P., et al. (2010) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2010.00871.x · Cited by 121 · see citing works
Studies on Cellulose Fermentation
Hungate, R. E. (1947) · Journal of Bacteriology · doi:10.1128/jb.53.5.631-645.1947 · Cited by 114 · see citing works
Relationship between rumen methanogens and methane production in dairy cows fed diets supplemented with a feed enzyme additive
Zhou, M., Chung, Y.-H., Beauchemin, K. A., Holtshausen, L., Oba, M., McAllister, T. A., & Guan, L. (2011) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2011.05126.x · Cited by 111 · see citing works
Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium
Kenters, N., Henderson, G., Jeyanathan, J., Kittelmann, S., & Janssen, P. H. (2011) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2010.10.011 · Cited by 108 · see citing works
Methanogenic Population and CH <sub>4</sub> Production in Swedish Dairy Cows Fed Different Levels of Forage
Danielsson, R., Schnürer, A., Arthurson, V., & Bertilsson, J. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.00675-12 · Cited by 108 · see citing works
Differences in the Rumen Methanogen Populations of Lactating Jersey and Holstein Dairy Cows under the Same Diet Regimen
King, E. E., Smith, R. P., St‐Pierre, B., & Wright, A. G. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05130-11 · Cited by 107 · see citing works
Effect of Methanobrevibacter smithii on Xylanolytic Activity of Anaerobic Ruminal Fungi
Joblin, K. N., Naylor, G. E., & Williams, A. G. (1990) · Applied and Environmental Microbiology · doi:10.1128/aem.56.8.2287-2295.1990 · Cited by 105 · see citing works
Control of Rumen Microbial Fermentation for Mitigating Methane Emissions from the Rumen
Mitsumori, M., & Sun, W. (2008) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.2008.r01 · Cited by 105 · see citing works
Methane Production in Ruminants and its Significance
Czerkawski, J. W. (2015) · World review of nutrition and dietetics · doi:10.1159/000387580 · Cited by 104 · see citing works
Archaeal abundance in post-mortem ruminal digesta may help predict methane emissions from beef cattle
Wallace, R. J., Rooke, J. A., Duthie, C.-A., Hyslop, J. J., Ross, D. W., McKain, N., de Souza, S. M., Snelling, T. J., Waterhouse, A., & Roehe, R. (2014) · Scientific Reports · doi:10.1038/srep05892 · Cited by 100 · see citing works
Self-citation
Metagenomic analysis of the rumen microbiome of steers with wheat-induced frothy bloat
Pitta, D. W., Pinchak, W. E., Indugu, N., Vecchiarelli, B., Sinha, R., & Fulford, J. D. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00689 · Cited by 100 · see citing works
Association of methanogenic bacteria with rumen protozoa
Krumholz, L. R., Forsberg, C. W., & Veira, D. M. (1983) · Canadian Journal of Microbiology · doi:10.1139/m83-110 · Cited by 96 · see citing works
Regional and age dependent changes in gene expression of Toll-like receptors and key antimicrobial defence molecules throughout the gastrointestinal tract of dairy calves
Malmuthuge, N., Li, M., Fries, P. N., Griebel, P. J., & Guan, L. L. (2012) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2012.01.010 · Cited by 89 · see citing works
Detection of methanogens and proteobacteria from a single cell of rumen ciliate protozoa
Irbis, C., & Ushida, K. (2004) · The Journal of General and Applied Microbiology · doi:10.2323/jgam.50.203 · Cited by 84 · see citing works
Distribution and estimation of anaerobic zoosporic fungi along the digestive tracts of sheep
Rezaeian, M., Beakes, G. W., & Parker, D. S. (2004) · Mycological Research · doi:10.1017/s0953756204000929 · Cited by 82 · see citing works
Internal Transcribed Spacer 1 Secondary Structure Analysis Reveals a Common Core throughout the Anaerobic Fungi (Neocallimastigomycota)
Koetschan, C., Kittelmann, S., Lu, J., Al-Halbouni, D., Jarvis, G. N., Müller, T., Wolf, M., & Janssen, P. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091928 · Cited by 80 · see citing works
Effect of progressive inoculation of fauna-free sheep with holotrich protozoa and total-fauna on rumen fermentation, microbial diversity and methane emissions
Belanche, A., de la Fuente, G., & Newbold, C. J. (2014) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiu026 · Cited by 74 · see citing works
Effect of defaunation on the loss of energy in wethers fed different quantities of cellulose and normal or steamflaked maize starch
Kreuzer, M., Kirchgeßner, M., & Muller, H. L. (1986) · Animal Feed Science and Technology · doi:10.1016/0377-8401(86)90114-8 · Cited by 74 · see citing works
Investigating the effect of two methane-mitigating diets on the rumen microbiome using massively parallel sequencing
Ross, E. M., Moate, P. J., Marett, L. C., Cocks, B., & Hayes, B. J. (2013) · Journal of Dairy Science · doi:10.3168/jds.2013-6766 · Cited by 69 · see citing works
Structures of free-living and protozoa-associated methanogen communities in the bovine rumen differ according to comparative analysis of 16S rRNA and mcrA genes
Tymensen, L. D., Beauchemin, K. A., & McAllister, T. A. (2012) · Microbiology · doi:10.1099/mic.0.057984-0 · Cited by 69 · see citing works
Methanogens associated with rumen ciliates
Tokura, M., Ushida, K., Miyazaki, K., & KOJIMA, Y. (2006) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.1997.tb00365.x · Cited by 66 · see citing works
RUMINANT NUTRITION SYMPOSIUM: Use of genomics and transcriptomics to identify strategies to lower ruminal methanogenesis1,2,3
McAllister, T. A., Meale, S. J., Valle, E., Guan, L., Zhou, M., Kelly, W. J., Henderson, G., Attwood, G. T., & Janssen, P. H. (2015) · Journal of Animal Science · doi:10.2527/jas.2014-8329 · Cited by 66 · see citing works
Effects of H 2 and Formate on Growth Yield and Regulation of Methanogenesis in Methanococcus maripaludis
Costa, K. C., Yoon, S. H., Pan, M., Burn, J. A., Baliga, N. S., & Leigh, J. A. (2013) · Journal of Bacteriology · doi:10.1128/jb.02141-12 · Cited by 66 · see citing works
Rôle of the rumen ciliate protozoa Polyplastron multivesiculatum, Entodinium sp. and Isotricha prostoma in the digestion of a mixed diet in sheep
Jouany, J. P., Zainab, B., Sénaud, J., et al. (1981) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:19810701 · Cited by 66 · see citing works
Diversity, abundance and novel 16S rRNA gene sequences of methanogens in rumen liquid, solid and epithelium fractions of Jinnan cattle
Pei, C.-X., Mao, S., Cheng, Y., & Zhu, W. (2009) · animal · doi:10.1017/s1751731109990681 · Cited by 60 · see citing works
Mitigation of greenhouse gas emissions from livestock production
Weiske, A., & Petersen, S. O. (2005) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2005.08.009 · Cited by 57 · see citing works
Methane production and substrate degradation by rumen microbial communities containing single protozoal species in vitro
Ranilla, M. J., Jouany, J. P., & Morgavi, D. P. (2007) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2007.02251.x · Cited by 57 · see citing works
In vitroInteractions between Rumen H2-Producing Cellulolytic Microorganisms and H2-Utilizing Acetogenic and Sulfate-Reducing Bacteria
Morvan, B., Rieu-Lesme, F., Fonty, G., & Gouet, P. (1996) · Anaerobe · doi:10.1006/anae.1996.0023 · Cited by 54 · see citing works
Intracellular prokaryotes in rumen ciliate protozoa: Detection by confocal laser scanning microscopy after in situ hybridization with fluorescent 16S rRNA probes
Lloyd, D., Williams, A. G., Amann, R., Hayes, A. J., Durrant, L., & Ralphs, J. R. (1996) · European Journal of Protistology · doi:10.1016/s0932-4739(96)80011-3 · Cited by 51 · see citing works
A re-appraisal of the diversity of the methanogens associated with the rumen ciliates
REGENSBOGENOVA, M., McEwan, N. R., JAVORSKY, P., Kišidayová, S., Michałowski, T., Newbold, C. J., Hackstein, J. H. P., & Pristaš, P. (2004) · FEMS Microbiology Letters · doi:10.1016/j.femsle.2004.07.049 · Cited by 49 · see citing works
Persistence of defaunation effects on digestion and methane production in ewes
Bird, S. H., Hegarty, R. S., & Woodgate, R. T. (2008) · Australian Journal of Experimental Agriculture · doi:10.1071/ea07298 · Cited by 47 · see citing works
Estimates of repeatability and heritability of methane production in sheep using portable accumulation chambers
Goopy, J. P., Robinson, D. L., Woodgate, R. T., et al. (2015) · Animal Production Science · doi:10.1071/an13370 · Cited by 47 · see citing works
A re-appraisal of the diversity of the methanogens associated with the rumen ciliates
Regensbogenova, M., McEwan, N. R., Javorsky, P., Kišidayová, S., Michałowski, T., Newbold, C. J., Hackstein, J. H. P., & Pristaš, P. (2004) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2004.tb09771.x · Cited by 47 · see citing works
Effects of the absence of protozoa from birth or from weaning on the growth and methane production of lambs
Hegarty, R. S., Bird, S. H., Vanselow, B. A., & Woodgate, R. T. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114508981435 · Cited by 46 · see citing works
Exploring rumen methanogen genomes to identify targets for methane mitigation strategies
Attwood, G. T., Altermann, E., Kelly, W. J., Leahy, S. C., Zhang, L., & Morrison, M. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.04.004 · Cited by 44 · see citing works
Community Structure Analysis of Methanogens Associated with Rumen Protozoa Reveals Bias in Universal Archaeal Primers
Tymensen, L. D., & McAllister, T. A. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.07994-11 · Cited by 39 · see citing works
The metabolism of rumen ciliate protozoa
Coleman, G. S. (1986) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1986.tb01864.x · Cited by 38 · see citing works
Reponses of sheep to a vaccination of entodinial or mixed rumen protozoal antigens to reduce rumen protozoal numbers
Williams, Y. J., Rea, S. M., Popovski, S., Pimm, C. L., Williams, A. J., Toovey, A. F., Skillman, L. C., & Wright, A. G. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507801553 · Cited by 37 · see citing works
Quantifying body water kinetics and fecal and urinary water output from lactating Holstein dairy cows
Appuhamy, J. A. D. R. N., Wagner‐Riddle, C., Casper, D. P., France, J., & Kebreab, E. (2014) · Journal of Dairy Science · doi:10.3168/jds.2013-7755 · Cited by 33 · see citing works
Differential recovery of bacterial and archaeal 16S rRNA genes from ruminal digesta in response to glycerol as cryoprotectant
McKain, N., Genç, B., Snelling, T. J., & Wallace, R. J. (2013) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2013.10.009 · Cited by 30 · see citing works
Self-citation
Molecular identification of rumen methanogens: Technologies, advances and prospects
Zhou, M., McAllister, T. A., & Guan, L. L. (2011) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2011.04.005 · Cited by 30 · see citing works
Potential Environmental Benefits of Residual Feed Intake as Strategy to Mitigate Methane Emissions in Sheep
Muro‐Reyes, A., Bañuelos, H. G., Diaz-Garci, L. H., et al. (2011) · Journal of Animal and Veterinary Advances · doi:10.3923/javaa.2011.1551.1556 · Cited by 29 · see citing works
Effect of cocultivation of ruminal chytrid fungi with Methanobrevibacter smithii on lucerne stem degradation and extracellular fungal enzyme activities
Joblin, K. N., & Williams, A. G. (1991) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.1991.tb00520.x · Cited by 28 · see citing works
Natural variation in methane emission of sheep fed on a lucerne pellet diet is unrelated to rumen ciliate community type
Kittelmann, S., Pinares-Patiño, C. S., Seedorf, H., Kirk, M. R., McEwan, J. C., & Janssen, P. H. (2016) · Microbiology · doi:10.1099/mic.0.000245 · Cited by 12 · see citing works
Use of genomics and transcriptomics to identify strategies to lower ruminal methanogenesis
McAllister, T. A. (2014) · 2014 ADSA-ASAS-CSAS Joint Annual Meeting · Cited by 10 · see citing works
Methane production in dairy cows
Danielsson, R. (2016) · Epsilon Open Archive (Sveriges lantbruksuniversitet biblioteket (Swedish University of Agricultural Sciences)) · Cited by 6 · see citing works

Flagged first, then by citations

Research works printed but not linked: 1

[36]Kittelmann S Seedorf H Walters WA Clemente JC Knight R Gordon JI Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities Plos One 2013 8 e103171 10.1371/journal.pone.0047879 PMC3568148 23408926 · DOI

Sorted by citations

The rumen microbiome: balancing food security and environmental impacts
Mizrahi, I., Wallace, R. J., & Moraïs, S. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00543-6 · Cited by 490 · see citing works
Self-citation
Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future
Huws, S. A., Creevey, C. J., Oyama, L. B., Mizrahi, I., Denman, S. E., Popova, M., Muñoz-Tamayo, R., Forano, E., Waters, S. M., Hess, M., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02161 · Cited by 487 · see citing works
Self-citation
A heritable subset of the core rumen microbiome dictates dairy cow productivity and emissions
Wallace, R. J., Sasson, G., Garnsworthy, P. C., Tapio, I., Gregson, E., Bani, P., Huhtanen, P., Bayat, A. R., Strozzi, F., Biscarini, F., et al. (2019) · Science Advances · doi:10.1126/sciadv.aav8391 · Cited by 410 · see citing works
Self-citation
Phytogenic Additives Can Modulate Rumen Microbiome to Mediate Fermentation Kinetics and Methanogenesis Through Exploiting Diet–Microbe Interaction
Hassan, F.-U., Arshad, M. A., Ebeid, H. M., Rehman, M. S.-U., Khan, M. S., Shahid, S., & Yang, C. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.575801 · Cited by 160 · see citing works
Invited Review: Methane Sources, Quantification, and Mitigation in Grazing Beef Systems
Thompson, L. R., & Rowntree, J. E. (2020) · Applied Animal Science · doi:10.15232/aas.2019-01951 · Cited by 112 · see citing works
Dietary supplemental plant oils reduce methanogenesis from anaerobic microbial fermentation in the rumen
Vargas, J. E., Andrés, S., López-Ferreras, L., Snelling, T. J., Yáñez-Ruíz, D. R., García-Estrada, C., & López, S. (2020) · Scientific Reports · doi:10.1038/s41598-020-58401-z · Cited by 113 · see citing works
Self-citation
Characterization of the ruminal fermentation and microbiome in lambs supplemented with hydrolysable and condensed tannins
Salami, S. A., Valenti, B., Bella, M., O ' Grady, M. N., Luciano, G., Kerry, J. P., Jones, E., Priolo, A., & Newbold, C. J. (2018) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiy061 · Cited by 91 · see citing works
Identification, comparison, and validation of robust rumen microbial biomarkers for methane emissions using diverse Bos taurus breeds and basal diets
Auffret, M. D., Stewart, R., Dewhurst, R. J., Duthie, C.-A., Rooke, J. A., Wallace, R. J., Freeman, T. C., Snelling, T. J., Watson, M., & Roehe, R. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02642 · Cited by 82 · see citing works
Self-citation
Comparative Analysis of the Microbiota Between Sheep Rumen and Rabbit Cecum Provides New Insight Into Their Differential Methane Production
Mi, L., Yang, B., Hu, X., Luo, Y., Liu, J., Yu, Z., & Wang, J. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00575 · Cited by 50 · see citing works
Natural plant-based additives can improve ruminant performance by influencing the rumen microbiome
Ornaghi, M., Prado, R. M., Ramos, T. R., Catalano, F. R., Mottin, C., Creevey, C. J., Huws, S. A., & Prado, I. N. (2020) · doi:10.21203/rs.3.rs-29748/v1 · Cited by 3 · see citing works

Methanogenesis pathways of methanogens and their responses to substrates and temperature in sediments from the South Yellow Sea
Chen, Y., Wu, N., Liu, C., et al. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.152645 · Cited by 43 · see citing works
Activity and distribution of methanogenic bacteria in a lake sediment.
Endo, G. (1992) · ENVIRONMENTAL SYSTEMS RESEARCH · doi:10.2208/proer1988.20.152 · Cited by 1 · see citing works
Latitudinal distribution of microbial communities in anaerobic biological stabilization ponds: effect of the mean annual temperature
Yuan, M., Zhu, J. K., Wang, C., Wu, M., Sun, F., Han, X., He, Y., & Wu, W. (2016) · Microbial Biotechnology · doi:10.1111/1751-7915.12407 · Cited by 4 · see citing works
Organic matter supply and bacterial community composition predict methanogenesis rates in temperate lake sediments
Bertolet, B. L., West, W. E., Armitage, D., et al. (2019) · Limnology and Oceanography Letters · doi:10.1002/lol2.10114 · Cited by 42 · see citing works
Methanogenesis control by employing various environmental stress conditions in two-chambered microbial fuel cells
Chae, K., Choi, M., Kim, K., et al. (2010) · Bioresource Technology · doi:10.1016/j.biortech.2010.02.035 · Cited by 199 · see citing works

Authors: Tapio, I., Snelling, T. J., Strozzi, F., & Wallace, R. J.
Affiliations: Natural Resources Institute Finland (FI)
University of Aberdeen (GB)
Parco Tecnologico Padano (IT)
Corresponding author: Wallace, R. John
ORCID: Tapio, Ilma
Snelling, Timothy J.
Strozzi, Francesco
Wallace, R. John
Venue: Journal of Animal Science and Biotechnology
Publisher: Springer Science and Business Media LLC
Published: 2017-01-19
Volume: 8
Issue: 1
Pages: 7-7
ISSN: 1674-9782 (ISSN-L)
2049-1891
DOI: 10.1186/s40104-017-0141-0
PMC: PMC5244708
OpenAlex: W2575397500
Cited by: 391
References: 112
Citations by year: 2026: 33 · 2025: 49 · 2024: 53 · 2023: 44 · 2022: 54 · 2021: 56 · 2020: 46 · 2019: 27 · 2018: 24 · 2017: 5
FWCI: 4.52
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Jukuri (Natural Resources Institute Finland (Luke)) (submittedVersion, cc-by)
Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
Funders: Seventh Framework Programme (289319)
Topics: Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Ruminant Nutrition and Digestive Physiology
Physical Sciences › Engineering › Building and Construction › Anaerobic Digestion and Biogas Production
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords: rumen microbiota, methane emissions, ruminant livestock, methanogenesis, Methanobrevibacter gottschalkii, rumen protozoa, hydrogen production, rumen bacteria, rumen archaea, rumen fungi, formate, Bacteroidetes, Proteobacteria, methane mitigation

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

The ruminal microbiome associated with methane emissions from ruminant livestock

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks