Hostname: page-component-6d856f89d9-sp8b6 Total loading time: 0 Render date: 2024-07-16T04:52:31.995Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversity of gut methanogens in herbivorous animals

Published online by Cambridge University Press:  27 April 2012

B. St-Pierre  and
A.-D. G. Wright
B. St-Pierre
Affiliation:
Department of Animal Science, The University of Vermont, 570 Main Street, Burlington, Vermont 05405, USA
A.-D. G. Wright*
Affiliation:
Department of Animal Science, The University of Vermont, 570 Main Street, Burlington, Vermont 05405, USA
*
†E-mail: agwright@uvm.edu
Get access

Abstract

The digestion of plant biomass by symbiotic microbial communities in the gut of herbivore hosts also results in the production of methane, a greenhouse gas that is released into the environment where it contributes to climate change. As methane is exclusively produced by methanogenic archaea, various research groups have devoted their efforts to investigate the population structure of symbiotic methanogens in the gut of herbivores. In this review, we summarized and compared currently available results from 16S rRNA gene clone library studies, which cover a broad range of hosts from ruminant livestock species to wild ruminants, camelids, marsupials, primates, birds and reptiles. Although gut methanogens are very diverse, they tend to be limited to specific phylogenetic groups. Overall, methanogens related to species of the genus Methanobrevibacter are the most highly represented archaea in the gut of herbivores. However, under certain conditions, archaea from more phylogenetically distant groups are the most prevalent, such as methanogens belonging to either the genus Methanosphaera, the order Methanomicrobiales or the Thermoplasmatales-Affiliated Lineage C Comparisons not only highlight the strong influence of host species and diet in the determination of the population structure of symbiotic methanogens, but also reveal other complex relationships, such as wide differences between breeds, as well as unexpected similarities between unrelated species. These observations strongly support the need for high throughput sequencing and metagenomic studies to gain further insight.

Keywords

herbivoregutrumenmethanogenarchaea
Type
Full Paper
Information
animal , Volume 7 , Issue s1: The 8th International Symposium on the Nutrition of Herbivores (ISNH8) 6 – 9th September 2011, Aberystwyth (UK) , March 2013 , pp. 49 - 56
Copyright
Copyright © The Animal Consortium 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

An, D, Dong, X, Dong, Z 2005. Prokaryote diversity in the rumen of yak (Bos grunniens) and Jinnan cattle (Bos taurus) estimated by 16S rDNA homology analyses. Anaerobe 11, 207–215.CrossRefGoogle ScholarPubMed
Balch, WE, Fox, CE, Magrum, LJ, Woese, CR, Wolfe, RS 1979. Methanogens: reevaluation of a unique biological group. Microbiological Reviews 43, 260–296.CrossRefGoogle ScholarPubMed
Chaudhary, PP, Sirohi, SK 2009. Dominance of Methanomicrobium phylotype in methanogen population present in Murrah buffaloes (Bubalus bubalis). Letters in Applied Microbiology 49, 274–277.CrossRefGoogle ScholarPubMed
Christian, KA, Tracy, CR, Porter, WP 1984. Diet, digestion, and food preferences of Galapagos land iguanas. Herpetologica 40, 205–212.Google Scholar
Eisenberg, JF, Muckenhirn, NA, Rundran, R 1972. The relation between ecology and social structure in primates. Science 176, 863–874.Google Scholar
Espinoza, RE, Wiens, JJ, Tracy, CR 2004. Recurrent evolution of herbivory in small, cold-climate lizards: breaking the ecophysiological rules of reptilian herbivory. Proceedings of the National Academy of Sciences of the United States of America 101, 16819–16824.CrossRefGoogle ScholarPubMed
Euzéby, JP 2012. List of Prokaryotic Names with Standing in Nomenclature. Retrieved February 02, 2012, from http://www.bacterio.cict.fr/.Google Scholar
Evans, PN, Hinds, LA, Sly, LI, McSweeney, CS, Morrison, M, Wright, A-DG 2009. Community composition and density of methanogens in the foregut of the Tammar wallaby (Macropus eugenii). Applied and Environmental Microbiology 75, 2598–2602.Google Scholar
Facey, HV, Northwood, KS, Wright, A-DG 2012. Molecular diversity of methanogens in fecal samples from zoo captive Sumatran orangutans (Pongo abelii). American Journal of Primatology 74, 408–413.Google Scholar
Franzolin, R, St-Pierre, B, Northwood, K, Wright, A-DG 2012. Analysis of rumen methanogen diversity in water buffaloes (Bubalus bubalis) under three different diets. Microbial Ecology (in press); doi: 10.1007/s00248-012-0007-0.Google Scholar
Fricke, WF, Seedorf, H, Henne, A, Kruer, M, Liesegang, H, Hedderich, R, Gottschalk, G, Thauer, RK 2006. The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. Journal of Bacteriology 188, 642–658.Google Scholar
Hackstein, JHP, Van Alen, T 1996. Fecal methanogens and vertebrate evolution. Evolution 50, 559–572.Google Scholar
Hong, PY, Wheeler, E, Cann, IKO, Mackie, RI 2011. Phylogenetic analysis of the fecal microbial community in herbivorous land and marine iguanas of the Galápagos Islands using 16S rRNA-based pyrosequencing. ISME Journal 5, 1461–1470.Google Scholar
Hook, SE, Northwood, KS, Wright, A-DG, McBride, BW 2009. Long-term monensin supplementation does not significantly affect the quantity or diversity of methanogens in the rumen of the lactating dairy cow. Applied and Environmental Microbiology 75, 374–380.Google Scholar
Hook, SE, Steele, MA, Northwood, KS, Wright, A-DG, McBride, BW 2011. Impact of high-concentrate feeding and low ruminal pH on methanogens and protozoa in the rumen of dairy cows. Microbial Ecology 62, 94–105.Google Scholar
Johnson, KA, Johnson, DE 1995. Methane emissions from cattle. Journal of Animal Science 73, 2483–2492.Google Scholar
Kim, M, Morrison, M, Yu, Z 2011. Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiology Ecology 76, 49–63.CrossRefGoogle ScholarPubMed
King, EE, Smith, RP, St-Pierre, B, Wright, A-DG 2011. Differences in the rumen methanogen populations of lactating Jersey and Holstein dairy cows under the same diet regimen. Applied and Environmental Microbiology 77, 5682–5687.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, 171–189.CrossRefGoogle ScholarPubMed
Nakamura, N, Amato, KR, Garber, P, Estrada, A, Mackie, RI, Gaskins, HR 2011. Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in palenque national park, Mexico. American Journal of Primatology 73, 909–919.Google Scholar
Pei, C-X, Mao, S-Y, Cheng, Y-F, Zhu, W-Y 2010. Diversity, abundance and novel 16S rRNA gene sequences of methanogens in rumen liquid, solid and epithelium fractions of Jinnan cattle. Animal 4, 20–29.Google Scholar
Prothero, DR, Schoch, RM 2002. Tylopods. In Horns, tusks, and flippers: the evolution of hoofed mammals (ed. DR Prothero and RM Schoch), pp. 45–56. John Hopkins University Press, Baltimore, MD.Google Scholar
Raskin, L, Stromley, JM, Rittmann, BE, Stahl, DA 1994. Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Applied and Environmental Microbiology 60, 1232–1240.CrossRefGoogle ScholarPubMed
Saengkerdsub, S, Anderson, RC, Wilkinson, HH, Kim, WK, Nisbet, DJ, Ricke, SC 2007. Identification and quantification of methanogenic archaea in adult chicken ceca. Applied and Environmental Microbiology 73, 353–356.Google Scholar
Shepherd, SA, Hawkes, MW 2005. Algal food preferences and seasonal foraging strategy of the marine iguana, Amblyrhynchus cristatus, on Santa Cruz, Galapagos. Bulletin of Marine Science 77, 51–72.Google Scholar
Singh, KM, Tripathi, AK, Pandya, PR, Parnerkar, S, Rank, DN, Kothari, RK, Joshi, CG 2012. Methanogen diversity in the rumen of Indian Surti buffalo (Bubalus bubalis), assessed by 16S rDNA analysis. Research in Veterinary Science 92, 451–455.Google Scholar
Skillman, LC, Evans, PN, Strompl, C, Joblin, KN 2006. 16S rDNA directed PCR primers and detection of methanogens in the bovine rumen. Letters in Applied Microbiology 42, 222–228.Google Scholar
Stevens, CE, Hume, ID 1995. Comparative physiology of the vertebrate digestive system, 2nd edition. Cambridge University Press, Cambridge.Google Scholar
St-Pierre, B, Wright, A-DG 2012. Molecular analysis of methanogenic archaea in the forestomach of the alpaca (Vicugna pacos). BMC Microbiology 12, 1.Google Scholar
Sundset, MA, Edwards, JE, Cheng, YF, Senosiain, RS, Fraile, MN, Northwood, KS, Præsteng, KE, Glad, T, Mathiesen, SD, Wright, A-DG 2009a. Molecular diversity of the rumen microbiome of Norwegian reindeer on natural summer pasture. Microbial Ecology 57, 335–348.Google Scholar
Sundset, MA, Edwards, JE, Cheng, YF, Senosiain, RS, Fraile, MN, Northwood, KS, Præsteng, KE, Glad, T, Mathiesen, SD, Wright, A-DG 2009b. Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea. FEMS Microbiology Ecology 70, 553–562.Google Scholar
Thorpe, A 2008. Enteric fermentation and ruminant eructation: the role (and control?) of methane in the climate change debate. Climatic Change 93, 407–431.CrossRefGoogle Scholar
Turnbull, KL, Smith, RP, St-Pierre, B, Wright, A-DG 2012. Molecular diversity of methanogens in fecal samples from Bactrian camels (Camelus bactrianus) at two zoos. Research in Veterinary Science; doi:10.1016/j.rvsc.2011.1008.1013.Google Scholar
Whitford, MF, Teather, RM, Forster, RJ 2001. Phylogenetic analysis of methanogens from the bovine rumen. BMC Microbiology 1, 1–5.Google Scholar
Wolin, MJ 1979. The rumen fermentation: a model for microbial interactions in anaerobic ecosystems. In Advances in Microbial Ecology (ed. M Alexander), vol. 3, pp. 49–77. Plenum Press, New York and London.Google Scholar
Wright, A-DG, Toovey, AF, Pimm, CL 2006. Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveal more uncultured novel archaea. Anaerobe 12, 134–139.Google Scholar
Wright, A-DG, Auckland, CH, Lynn, DH 2007. Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Applied and Environmental Microbiology 73, 4206–4210.Google Scholar
Wright, A-DG, Ma, X, Obispo, NE 2008. Methanobrevibacter phylotypes are the dominant methanogens in sheep from Venezuela. Microbial Ecology 56, 390–394.Google Scholar
Wright, A-DG, Northwood, KS, Obispo, NE 2009. Rumen-like methanogens identified from the crop of the folivorous South American bird, the hoatzin (Opisthocomus hoazin). ISME Journal 3, 1120–1126.Google Scholar
Wright, A-DG, Williams, AJ, Winder, B, Christophersen, CT, Rodgers, SL, Smith, KD 2004. Molecular diversity of rumen methanogens from sheep in Western Australia. Applied and Environmental Microbiology 70, 1263–1270.Google Scholar
Yamamoto, N, Otawa, K, Nakai, Y 2010. Diversity and abundance of ammonia-oxidizing bacteria and ammonia-oxidizing archaea during cattle manure composting. Microbial Ecology 60, 807–815.CrossRefGoogle ScholarPubMed