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Microbial Ecology

, Volume 66, Issue 4, pp 879–888 | Cite as

Differences in the Methanogen Population Exist in Sika Deer (Cervus nippon) Fed Different Diets in China

  • Zhi Peng Li
  • Han Lu Liu
  • Chun Ai Jin
  • Xue Zhe Cui
  • Yi Jing
  • Fu He Yang
  • Guang Yu Li
  • André-Denis G. Wright
Environmental Microbiology

Abstract

Understanding the methanogen structure from sika deer (Cervus nippon) in China may be beneficial to methane mitigation. In the present preliminary study, we investigated the methanogen community in the rumen of domesticated sika deer fed either tannin-rich plants (oak leaf, OL group) or corn stalk (CS group) using 16S rRNA gene clone libraries. Overall, we obtained 197 clone sequences, revealing 146 unique phylotypes, which were assigned to 36 operational taxonomic units at the species level (98 % identity). Methanogens related to the genus Methanobrevibacter were the predominant phylotypes representing 83.9 % (OL library) and 85.9 % (CS library) of the clones. Methanobrevibacter millerae was the most abundant species in both libraries, but the proportion of M. millerae-related clones in the CS library was higher than in the OL library (69.5 and 51.4 %, respectively). Moreover, Methanobrevibacter wolinii-related clones (32.5 %) were predominant in the OL library. Methanobrevibacter smithii-related clones and Methanobrevibacter ruminantium-related clones accounted for 6.5 and 6.6 % in the CS library, respectively. However, these clones were absent from the OL library. The concentrations of butyrate and total short-chain fatty acids (SCFAs) were significantly higher in the OL group, but the concentrations of acetate, propionate, and valerate and the acetate to propionate ratio in the OL group were not significantly different between the two groups. Tannin-rich plants may have affected the distribution of genus Methanobrevibacter phylotypes at the species level and the concentration and composition of SCFAs.

Keywords

Condensed Tannin Sika Deer Corn Stalk Methanobrevibacter Methanobacteriales 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

OTU

Operational taxonomic units

SCFAs

Short-chain fatty acids

DGGE

Denaturing gradient gel electrophoresis

CAAS

Chinese Academy of Agricultural Sciences

Notes

Acknowledgments

This work is supported by a Young Researcher funded project (201101086), Science and Technology Development project (20090238), a Leading Talent and Creative Team project (20121810), and Natural Science Foundation (20130101104JC), all from Jilin province. The Ministry of Agriculture Public Sector (Agriculture) Special Research Project (200903014) and Key Projects in the National Science & Technology Pillar Program (2011BAI03B02).

References

  1. 1.
    Gill M, Smith P, Wilkinson JM (2010) Mitigating climate change: the role of domestic livestock. Animal 4:323–333. doi: 10.1017/S1751731109004662 CrossRefPubMedGoogle Scholar
  2. 2.
    Johnson KA, Johnson DE (1995) Methane emissions from cattle. J Anim Sci 73:2483–2492PubMedGoogle Scholar
  3. 3.
    Li ZP, Liu HL, Li GY, Bao K, Wang KY, Xu C, Yang YF, Yang FH, Wright ADG (2013) Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic sika deer (Cervus nippon) in China. BMC Microbiol 13:151. doi: 10.1186/1471-2180-13-151 PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6:121–131. doi: 10.1038/nrmicro1817 CrossRefPubMedGoogle Scholar
  5. 5.
    Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, North American Consortium for Rumen Bacteria, Coutinho PM, Henrissat B, Nelson KE (2010) Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb Ecol 60:721–729. doi: 10.1007/s00248-010-9692-8 CrossRefPubMedGoogle Scholar
  6. 6.
    Strobel HJ (1992) Vitamin B12-dependent propionate production by the ruminal bacterium Prevotella ruminicola 23. Appl Environ Microbiol 58:2331–2333PubMedCentralPubMedGoogle Scholar
  7. 7.
    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. Br J Nutr 108:482–491. doi: 10.1017/S0007114511005794 CrossRefPubMedGoogle Scholar
  8. 8.
    Shinkai T, Enishi O, Mitsumori M, Higuchi K, Kobayashi Y, Takenaka A, Nagashima K, Mochizuki M, Kobayashi Y (2012) Mitigation of methane production from cattle by feeding cashew nut shell liquid. J Dairy Sci 95:5308–5316. doi: 10.3168/jds.2012-5554 CrossRefPubMedGoogle Scholar
  9. 9.
    Yang Y (2010) Effects of tannins on the nutrition utilization and growth of young sika deer (Cervus nippon). Master’s thesis, Chinese Academy of Agricultural Sciences (in Chinese)Google Scholar
  10. 10.
    Ichimura Y, Yamano H, Takano T, Koike S, Kobayashi Y, Tanaka K, Ozaki N, Suzuki M, Okada H, Yamanaka M (2004) Rumen microbes and fermentation of wild sika deer on the Shiretoko Peninsula of Hokkaido Island, Japan. Ecol Res 19:389–395. doi: 10.1111/j.1440-1703.2004.00649.x CrossRefGoogle Scholar
  11. 11.
    Hiura T, Hashidoko Y, Kobayashi Y, Tahara S (2010) Effective degradation of tannic acid by immobilized rumen microbes of a sika deer (Cervus nippon yesoensis) in winter. Anim Feed Sci Technol 155:1–8CrossRefGoogle Scholar
  12. 12.
    Tan HY, Sieo CC, Lee CM, Abdullah N, Liang JB, Ho YW (2011) Diversity of bovine rumen methanogens in vitro in the presence of condensed tannins, as determined by sequence analysis of 16S rRNA gene library. J Microbiol 49:492–498. doi: 10.1007/s12275-011-0319-7 CrossRefPubMedGoogle Scholar
  13. 13.
    Puchala R, Min BR, Goetsch AL, Sahlu T (2005) The effect of a condensed tannin-containing forage on methane emission by goats. J Anim Sci 83:182–186PubMedGoogle Scholar
  14. 14.
    Tiemann TT, Lascano CE, Wettstein HR, Mayer AC, Kreuzer M, Hess HD (2008) Effect of the tropical tannin-rich shrub legumes Calliandra calothyrsus and Flemingia macrophylla on methane emission and nitrogen and energy balance in growing lambs. Animal 2:790–799. doi: 10.1017/S1751731108001791 CrossRefPubMedGoogle Scholar
  15. 15.
    Liu H, Vaddella V, Zhou D (2011) Effects of chestnut tannins and coconut oil on growth performance, methane emission, ruminal fermentation, and microbial populations in sheep. J Dairy Sci 94:6069–6077. doi: 10.3168/jds.2011-4508 CrossRefPubMedGoogle Scholar
  16. 16.
    Carulla JE, Kreuzer M, Machmuller A, Hess HD (2005) Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Aust J Agric Res 56:961–970CrossRefGoogle Scholar
  17. 17.
    Cieslak A, Zmora P, Pers-Kamczyc E, Szumacher-Strabel M (2012) Effects of tannins source (Vaccinium vitis idaea L.) on rumen microbial fermentation in vivo. Anim Feed Sci Technol 176:102–106. doi: 10.1016/j.anifeedsci.2012.07.012 CrossRefGoogle Scholar
  18. 18.
    Radovan GA, Sevilla CC, Capitan SS, Vega RSA, Alcantara AJ, Yebron MGN (2013) Molecular diversity of rumen methanogens in cattle in response to dietary tannin. Philipp J Vet Anim Sci 39:21–30Google Scholar
  19. 19.
    Tan HY, Sieo CC, Abdullah N, Liang JB, Huang XD, Ho YW (2011) Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro. Anim Feed Sci Technol 169:185–193CrossRefGoogle Scholar
  20. 20.
    Wright ADG, Pimm C (2003) Improved strategy for presumptive identification of methanogens using 16S riboprinting. J Microbiol Methods 55:337–349CrossRefPubMedGoogle Scholar
  21. 21.
    Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319CrossRefPubMedGoogle Scholar
  22. 22.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralCrossRefPubMedGoogle Scholar
  25. 25.
    Wright ADG, Northwood KS, Obispo NE (2009) Rumen-like methanogens identified from the crop of the folivorous South American bird, the hoatzin (Opisthocomus hoazin). ISME J 3:1120–1126. doi: 10.1038/ismej.2009.41 CrossRefPubMedGoogle Scholar
  26. 26.
    Wright ADG, Ma X, Obispo NE (2008) Methanobrevibacter phylotypes are the dominant methanogens in sheep from Venezuela. Microb Ecol 56:390–394. doi: 10.1007/s00248-007-9351-x CrossRefPubMedGoogle Scholar
  27. 27.
    Hook SE, Wright ADG, McBride BW (2010) Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010:945785. doi: 10.1155/2010/945785 PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Evans PN, Hinds LA, Sly LI, McSweeney CS, Morrison M, Wright ADG (2009) Community composition and density of methanogens in the foregut of the Tammar wallaby (Macropus eugenii). Appl Environ Microbiol 75:2598–2602. doi: 10.1128/AEM.02436-08 PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Whitford MF, Teather RM, Forster RJ (2001) Phylogenetic analysis of methanogens from the bovine rumen. BMC Microbiol 1:5PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    King EE, Smith RP, St-Pierre B, Wright ADG (2011) Differences in the rumen methanogen populations of lactating Jersey and Holstein dairy cows under the same diet regimen. Appl Environ Microbiol 77:5682–5687. doi: 10.1128/AEM.05130-11 PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Kong Y, Xia Y, Seviour R, Forster R, McAllister TA (2013) Biodiversity and composition of methanogenic populations in the rumen of cows fed alfalfa hay or triticale straw. FEMS Microbiol Ecol 84:302–315. doi: 10.1111/1574-6941.12062 CrossRefPubMedGoogle Scholar
  32. 32.
    Wright ADG, Auckland CH, Lynn DH (2007) Molecular diversity of methanogens in feedlot cattle from Ontario and Prince Edward Island, Canada. Appl Environ Microbiol 73:4206–4210. doi: 10.1128/AEM.00103-07 PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Sundset MA, Edwards JE, Cheng YF, Senosiain RS, Fraile MN, Northwood KS, Praesteng KE, Glad T, Mathiesen SD, Wright ADG (2009) Molecular diversity of the rumen microbiome of Norwegian reindeer on natural summer pasture. Microb Ecol 57:335–348. doi: 10.1007/s00248-008-9414-7 CrossRefPubMedGoogle Scholar
  34. 34.
    Jeyanathan J, Kirs M, Ronimus RS, Hoskin SO, Janssen PH (2011) Methanogen community structure in the rumens of farmed sheep, cattle and red deer fed different diets. FEMS Microbiol Ecol 76:311–326. doi: 10.1111/j.1574-6941.2011.01056.x CrossRefPubMedGoogle Scholar
  35. 35.
    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. Appl Environ Microbiol 78:8245–8253. doi: 10.1128/AEM.02193-12 PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Janssen PH, Kirs M (2008) Structure of the archaeal community of the rumen. Appl Environ Microbiol 74:3619–3625. doi: 10.1128/AEM.02812-07 PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Wright ADG, Toovey AF, Pimm CL (2006) Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveal more uncultured novel archaea. Anaerobe 12:134–139. doi: 10.1016/j.anaerobe.2006.02.002 CrossRefPubMedGoogle Scholar
  38. 38.
    Chaudhary PP, Sirohi SK, Saxena J (2012) Diversity analysis of methanogens in rumen of Bubalus bubalis by 16S riboprinting and sequence analysis. Gene 493:13–17. doi: 10.1016/j.gene.2011.11.041 CrossRefPubMedGoogle Scholar
  39. 39.
    Sundset MA, Edwards JE, Cheng YF, Senosiain RS, Fraile MN, Northwood KS, Praesteng KE, Glad T, Mathiesen SD, Wright ADG (2009) Rumen microbial diversity in Svalbard reindeer, with particular emphasis on methanogenic archaea. FEMS Microbiol Ecol 70:553–562. doi: 10.1111/j.1574-6941.2009.00750.x CrossRefPubMedGoogle Scholar
  40. 40.
    Huang XD, Tan HY, Long R, Liang JB, Wright ADG (2012) Comparison of methanogen diversity of yak (Bos grunniens) and cattle (Bos taurus) from the Qinghai–Tibetan plateau, China. BMC Microbiol 12:237. doi: 10.1186/1471-2180-12-237 PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    McSweeney C, Mackie R (2012) Micro-organisms and ruminant digestion: state of knowledge, trends and future prospects. FAO (Food and Agriculture Organization of the United Nations): 7th Session of the Intergovernmental Technical Working Group on Animal Genetic Resources for Food and Agriculture. Targets and indicators for animal genetic resources. 24–26 October 2012. Available at http://www.fao.org/docrep/016/me992e/me992e.pdf
  42. 42.
    McSweeney C, Kang S, Gagen E, Davis C, Morrison M, Denman S (2009) Recent developments in nucleic acid based techniques for use in rumen manipulation. Rev Bras Zootec-Braz J Anim Sci 38:341–351CrossRefGoogle Scholar
  43. 43.
    Mohammed R, Zhou M, Koenig KM, Beauchemin KA, Guan LL (2011) Evaluation of rumen methanogen diversity in cattle fed diets containing dry corn distillers grains and condensed tannins using PCR-DGGE and qRT-PCR analyses. Anim Feed Sci Technol 166–67:122–131CrossRefGoogle Scholar
  44. 44.
    Zhou M, Hernandez-Sanabria E, le Guan L (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. Appl Environ Microbiol 76:3776–3786. doi: 10.1128/AEM.00010-10 PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    St-Pierre B, Wright ADG (2012) Molecular analysis of methanogenic archaea in the forestomach of the alpaca (Vicugna pacos). BMC Microbiol 12:1. doi: 10.1186/1471-2180-12-1 PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Pinares-Patino CS, Ulyatt MJ, Waghorn GC, Lassey KR, Barry TN, Holmes CW, Johnson DE (2003) Methane emission by alpaca and sheep fed on lucerne hay or grazed on pastures of perennial ryegrass/white clover or birdsfoot trefoil. J Agric Sci 140:215–226CrossRefGoogle Scholar
  47. 47.
    Zhou M, Hernandez-Sanabria E, Guan LL (2009) Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Appl Environ Microbiol 75:6524–6533. doi: 10.1128/AEM.02815-08 PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Zhou M, Chung YH, Beauchemin KA, Holtshausen L, Oba M, McAllister TA, Guan LL (2011) Relationship between rumen methanogens and methane production in dairy cows fed diets supplemented with a feed enzyme additive. J Appl Microbiol 111:1148–1158CrossRefPubMedGoogle Scholar
  49. 49.
    Li G, Gao X, Zhao J, Gao Y (1998) Studies on year-periodic changes of protozoal counts, pH values in the rumen of sika deer. Chin J Anim Sci 34:9–11 (in Chinese)Google Scholar
  50. 50.
    Ohene-Adjei S, Teather RM, Ivan M, Forster RJ (2007) Postinoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Appl Environ Microbiol 73:4609–4618. doi: 10.1128/AEM.02687-06 PubMedCentralCrossRefPubMedGoogle Scholar
  51. 51.
    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 of sheep. J Anim Sci 89:783–791. doi: 10.2527/jas.2010-2947 CrossRefPubMedGoogle Scholar
  52. 52.
    Patra AK, Saxena J (2011) Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. J Sci Food Agric 91:24–37. doi: 10.1002/jsfa.4152 CrossRefPubMedGoogle Scholar
  53. 53.
    Leahy SC, Kelly WJ, Li D, Li Y, Altermann E, Lambie SC, Cox F, Attwood GT (2013) The complete genome sequence of Methanobrevibacter sp. AbM4. Stand Genomic Sci 8:215–227. doi: 10.4056/sigs.3977691 PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Wang YY, Zhang YL, Wang JB, Meng L (2009) Effects of volatile fatty acid concentrations on methane yield and methanogenic bacteria. Biomass Bioenergy 33:848–853. doi: 10.1016/j.biombioe.2009.01.007 CrossRefGoogle Scholar
  55. 55.
    Franzolin R, St-Pierre B, Northwood K, Wright ADG (2012) Analysis of rumen methanogen diversity in water buffaloes (Bubalus bubalis) under three different diets. Microb Ecol 64:131–139. doi: 10.1007/s00248-012-0007-0 CrossRefPubMedGoogle Scholar
  56. 56.
    Danielsson R, Schnurer A, Arthurson V, Bertilsson J (2012) Methanogenic population and CH4 production in Swedish dairy cows fed different levels of forage. Appl Environ Microbiol 78:6172–6179. doi: 10.1128/AEM.00675-12 PubMedCentralCrossRefPubMedGoogle Scholar
  57. 57.
    Newbold CJ, Lopez S, Nelson N, Ouda JO, Wallace RJ, Moss AR (2005) Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro. Br J Nutr 94:27–35CrossRefPubMedGoogle Scholar
  58. 58.
    Animut G, Puchala R, Goetsch AL, Patra AK, Sahlu T, Varel VH, Wells J (2008) Methane emission by goats consuming diets with different levels of condensed tannins from Lespedeza. Anim Feed Sci Technol 144:212–227. doi: 10.1016/j.anifeedsci.2007.10.014 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Zhi Peng Li
    • 1
  • Han Lu Liu
    • 1
  • Chun Ai Jin
    • 1
  • Xue Zhe Cui
    • 1
  • Yi Jing
    • 1
  • Fu He Yang
    • 1
  • Guang Yu Li
    • 1
  • André-Denis G. Wright
    • 2
  1. 1.Department of Economical Animal Nutrition and Feed Science, Institute of Special Animal and Plant SciencesChinese Academy of Agricultural SciencesJilinChina
  2. 2.Department of Animal ScienceUniversity of VermontBurlingtonUSA

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