Advertisement

Methane Emission, Rumen Fermentation, and Microbial Community Response to a Nitrooxy Compound in Low-Quality Forage Fed Hu Sheep

  • Fei Xie
  • Lingli Zhang
  • Wei JinEmail author
  • Zhenxiang Meng
  • Yanfen Cheng
  • Jing Wang
  • Weiyun Zhu
Article

Abstract

The effects of nitroglycerine (NG) on the rumen methane emission, fermentation, and microbial community of Hu sheep were investigated. Eight sheep were fed NG (100 mg/head/day); another eight sheep served as controls. NG decreased methane emission of Hu sheep by ~ 19.3% (P < 0.05) without adversely affecting the production performance or rumen fermentation (P > 0.05). The alpha and beta diversity indexes of the bacterial and archaeal community showed no significant differences (P > 0.05). The dominant methanogenic species was the Methanobrevibacter gottschalkii clade, accounting for ~ 60%, followed by the Methanobrevibacter boviskoreani and Methanobrevibacter ruminantium clades. Prevotella 1 was the most dominant bacterial genus, accounting for ~ 42%, followed by the Rikenellaceae RC9 and Bacteroidales BS11 gut groups. In addition, pearson correlation analysis showed a few Methanomassiliicoccales species significantly correlated with several bacterial genera (P < 0.05).

Notes

Acknowledgements

This research was supported by the National Natural Science Foundation of China (31872381), and the Fundamental Research Funds for the Central Universities (KYZ201854).

Compliance with Ethical Standards

Competing interests

The authors have declared that no competing interests exist.

Supplementary material

284_2019_1644_MOESM1_ESM.docx (279 kb)
Supplementary material 1 (DOCX 279 KB)

References

  1. 1.
    Association of Official Analytical Chemists (AOAC) (2000) Official methods of analysis of AOAC international, 17th edn. AOAC International, GaithersburgGoogle Scholar
  2. 2.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
  3. 3.
    Cersosimo LM, Lachance H, St-Pierre B, Van Hoven W, Wright ADG (2015) Examination of the rumen bacteria and methanogenic archaea of wild impalas (Aepyceros melampus melampus) from Pongola, South Africa. Microb Ecol 69:577–585.  https://doi.org/10.1007/s00248-014-0521-3 CrossRefGoogle Scholar
  4. 4.
    Dennis KL, Wang Y, Blatner NR, Wang S, Saadalla A, Trudeau E, Roers A, Weaver CT, Lee JJ, Gilbert JA (2013) Adenomatous polyps are driven by microbe-instigated focal inflammation and are controlled by IL-10-producing T cells. Cancer Res 73:5905–5913.  https://doi.org/10.1158/0008-5472.CAN-13-1511 CrossRefGoogle Scholar
  5. 5.
    Duin EC, Wagner T, Shima S, Prakash D, Cronin B, Yáñez-Ruiz DR, Duval S, Rümbeli R, Stemmler RT, Thauer RK, Kindermann M (2016) Mode of action uncovered for the specific reduction of methane emissions from ruminants by the small molecule 3-nitrooxypropanol. Proc Natl Acad Sci USA 113:6172–6177.  https://doi.org/10.1073/pnas.1600298113 CrossRefGoogle Scholar
  6. 6.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998.  https://doi.org/10.1038/nmeth.2604 CrossRefGoogle Scholar
  7. 7.
    Jameson E, Fu T, Brown IR, Paszkiewicz K, Purdy KJ, Frank S, Chen Y (2016) Anaerobic choline metabolism in microcompartments promotes growth and swarming of Proteus mirabilis. Environ Microbiol 18:2886–2898.  https://doi.org/10.1111/1462-2920.13059 CrossRefGoogle Scholar
  8. 8.
    Jiang Y, Ogunade IM, Arriola KG, Qi M, Vyas D, Staples CR, Adesogan AT (2017) Effects of the dose and viability of Saccharomyces cerevisiae. 2. Ruminal fermentation, performance of lactating dairy cows, and correlations between ruminal bacteria abundance and performance measures. J Dairy Sci 100:8102–8118.  https://doi.org/10.3168/jds.2016-12371 CrossRefGoogle Scholar
  9. 9.
    Jin W, Meng Z, Wang J, Cheng Y, Zhu W (2017) Effect of nitrooxy compounds with different molecular structures on the rumen methanogenesis, metabolic profile, and methanogenic community. Curr Microbiol 74:891–898.  https://doi.org/10.1007/s00284-017-1261-7 CrossRefGoogle Scholar
  10. 10.
    Johnson KA, Johnson DE (1995) Methane emissions from cattle. J Anim Sci 73:2483–2492.  https://doi.org/10.2527/1995.7382483x CrossRefGoogle Scholar
  11. 11.
    Kröninger L, Gottschling J, Deppenmeier U (2017) Growth characteristics of Methanomassiliicoccus luminyensis and expression of methyltransferase encoding genes. Archaea 2017:1–12.  https://doi.org/10.1155/2017/2756573 CrossRefGoogle Scholar
  12. 12.
    Li Y, Leahy SC, Jeyanathan J, Henderson G, Cox F, Altermann E, Kelly WJ, Lambie SC, Janssen PH, Rakonjac J, Attwood GT (2016) The complete genome sequence of the methanogenic archaeon ISO4-H5 provides insights into the methylotrophic lifestyle of a ruminal representative of the Methanomassiliicoccales. Stand Genomic Sci 11:59.  https://doi.org/10.1186/s40793-016-0183-5 CrossRefGoogle Scholar
  13. 13.
    Makkar HPS, Sharma OP, Dawra RK, Negi SS (1982) Simple determination of microbial protein in rumen liquor. J Dairy Sci 65:2170–2173.  https://doi.org/10.3168/jds.S0022-0302(82)82477-6 CrossRefGoogle Scholar
  14. 14.
    Mao S, Zhang M, Liu J, Zhu W (2015) Characterising the bacterial microbiota across the gastrointestinal tracts of dairy cattle: membership and potential function. Sci Rep-UK 5:16116.  https://doi.org/10.1038/srep16116 CrossRefGoogle Scholar
  15. 15.
    Martínez-del CA, Bodea S, Hamer HA, Marks JA, Haiser HJ, Turnbaugh PJ, Balskus EP (2015) Characterization and detection of a widely distributed gene cluster that predicts anaerobic choline utilization by human gut bacteria. Mbio 6:e00042–e00015.  https://doi.org/10.1128/mBio.00042-15 Google Scholar
  16. 16.
    Martínez-Fernández G, Abecia L, Arco A, Cantalapiedra-Hijar G, Martín-García AI, Molina-Alcaide E, Kindermann M, Duval S, Yáñez-Ruiz DR (2014) Effects of ethyl-3-nitrooxy propionate and 3-nitrooxypropanol on ruminal fermentation, microbial abundance, and methane emissions in sheep. J Dairy Sci 97:3790–3799.  https://doi.org/10.3168/jds.2013-7398 CrossRefGoogle Scholar
  17. 17.
    McAllister TA, Cheng KJ, Okine EK, Mathison GW (1996) Dietary, environmental and microbiological aspects of methane production in ruminants. J Anim Sci 76:231–243.  https://doi.org/10.4141/cjas.96-035 Google Scholar
  18. 18.
    Mi L, Yang B, Hu X, Luo Y, Liu J, Yu Z, Wang J (2018) Comparative analysis of the microbiota between sheep rumen and rabbit cecum provides new insight into their differential methane production. Front Microbiol 9:575.  https://doi.org/10.3389/fmicb.2018.00575 CrossRefGoogle Scholar
  19. 19.
    Miyazaki K, Martin JC, Marinsek-Logar R, Flint HJ (1997) Degradation and utilization of xylans by the rumen anaerobe Prevotella bryantii (formerly P. ruminicola subsp. brevis) B(1)4. Anaerobe 3:373.  https://doi.org/10.1006/anae.1997.0125 CrossRefGoogle Scholar
  20. 20.
    Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, 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.  https://doi.org/10.1007/s00248-010-9692-8 CrossRefGoogle Scholar
  21. 21.
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596.  https://doi.org/10.1093/nar/gks1219 CrossRefGoogle Scholar
  22. 22.
    Roberts AB, Gu X, Buffa JA, Hurd AG, Wang Z, Zhu W, Gupta N, Skye SM, Cody DB, Levison BS, Barrington WT, Russell MW, Reed JM, Duzan A, Lang JM, Fu X, Li L, Myers AJ, Rachakonda S, DiDonato JA, Brown JM, Gogonea V, Lusis AJ, Garcia-Garcia JC, Hazen SL (2018) Development of a gut microbe-targeted nonlethal therapeutic to inhibit thrombosis potential. Nat Med 24:1407–1417.  https://doi.org/10.1038/s41591-018-0128-1 CrossRefGoogle Scholar
  23. 23.
    Seedorf H, Kittelmann S, Henderson G, Janssen PH (2014) RIM-DB: a taxonomic framework for community structure analysis of methanogenic archaea from the rumen and other intestinal environments. PeerJ 2:e494.  https://doi.org/10.7717/peerj.494 CrossRefGoogle Scholar
  24. 24.
    Wallace RJ, Mckain N, Broderick GA, Rode LM, Walker ND, Newbold CJ, Kopecny J (1997) Peptidases of the rumen bacterium, Prevotella ruminicola. Anaerobe 3:35.  https://doi.org/10.1006/anae.1996.0065 CrossRefGoogle Scholar
  25. 25.
    Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974.  https://doi.org/10.1021/ac60252a045 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Fei Xie
    • 1
    • 2
  • Lingli Zhang
    • 1
    • 3
  • Wei Jin
    • 1
    • 2
    Email author
  • Zhenxiang Meng
    • 1
    • 2
  • Yanfen Cheng
    • 1
    • 2
  • Jing Wang
    • 1
    • 2
  • Weiyun Zhu
    • 1
    • 2
  1. 1.Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingChina
  2. 2.National Center for International Research on Animal Gut NutritionNanjing Agricultural UniversityNanjingChina
  3. 3.Shantou University Medical CollegeShantouChina

Personalised recommendations