Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Effect of rhubarb (Rheum spp.) root on in vitro and in vivo ruminal methane production and a bacterial community analysis based on 16S rRNA sequence

Kyoung Hoon Kim A B H * , Selvaraj Arokiyaraj B * , Jinwook Lee C , Young Kyoon Oh C , Ho Young Chung D , Gwi-Deuk Jin E , Eun Bae Kim E , Eun Kyoung Kim F , Yoonseok Lee B and Myunggi Baik G
+ Author Affiliations
- Author Affiliations

A Graduate School of International Agricultural Technology, Seoul National University, Pyeongchang, Republic of Korea.

B Institute of Green Bioscience and Technology, Seoul National University, Pyeongchang, Republic of Korea.

C Department of Animal Nutrition and Physiology, National Institute of Animal Science, RDA, Jeonju, Republic of Korea.

D Animal Genomics and Bioinformatics Division, National Institute of Animal Science, RDA, Jeonju, Republic of Korea.

E Department of Animal Life Science, Kangwon National University, Chuncheon, Republic of Korea.

F Division of Food Bio Science, KonKuk University, Chungju, Republic of Korea.

G Department of Agricultural Biotechnology and Research Institute of Agriculture and Life Sciences, Seoul National University, Seoul, Republic of Korea.

H Corresponding author. Email: khhkim@snu.ac.kr

Animal Production Science 56(3) 402-408 https://doi.org/10.1071/AN15585
Submitted: 14 September 2015  Accepted: 30 November 2015   Published: 9 February 2016

Abstract

The objective of this study was to evaluate the anti-methanogenic effect of rhubarb (Rheum spp.) on in vitro, in vivo, and bacterial community composition using Quantitative Insights into Microbial Ecology sequencing. Rhubarb root powder was tested at different concentrations (0, 0.33, 0.67, and 1.33 g/L) in vitro, and all incubations were carried out in triplicate two runs on separate days. Concentrations of 0.67 and 1.33 g/L rhubarb significantly (P < 0.05) reduced methane production and the acetate : propionate ratio compared with those of the Control, without adverse effects on total volatile fatty acids and total gas production. In the second in vivo trial, four Hanwoo (Korean native) steers (live bodyweight, 556 ± 46 kg) with a ruminal cannula were housed individually in metabolic stalls and fed a basal diet twice daily in equal amounts at 0900 hours and 2100 hours. The before rhubarb treatment (before treatment) duration was 24 days for all steers; 14 days were used for diet adaptation and 10 days were used for gas samples collected 1, 2, and 3 h after the morning feeding on Days 3, 5, 7, and 9. We used three syringe needles passed through the ruminal cannula stopper at different time points as a simple and rapid method to sample rumen gas. Thereafter, three mesh bags containing 30 g of sliced rhubarb root each were placed at different depths in the rumen of each steer for 14 days (after treatment), and gas samples were collected on Days 4, 7, 10, 12, and 13. The results showed a significant (P < 0.05) decrease in methane concentration from the rhubarb-treated steers and provide the evidence that this method would be useful for in vivo screening of anti-methanogenic feed additives or plant material. Furthermore, 16s RNA sequencing after treatment showed increases in the numbers of Prevotella, and Lactobacillus, but decreases in Methanobrevibacter. In conclusion, rhubarb had an anti-methanogenic effect in vitro and in vivo, and the increase in the number of Prevotella shifted ruminal fermentation towards propionate production.

Additional keywords: bacterial community, beef cattle, rhubarb, ruminal methane.


References

Aly MM, Gumgumjee NM (2011) Antimicrobial efficacy of Rheum palmatum, Curcuma longa and Alpinia officinarum extracts. African Journal of Biotechnology 10, 12058–12063.

Bodas R, López S, Fernández M, González RG, Rodríguez AB, Wallace RJ, González JS (2008) In vitro screening of the potential of numerous plant species as antimethanogenic feed additives for ruminants. Animal Feed Science and Technology 145, 245–258.
In vitro screening of the potential of numerous plant species as antimethanogenic feed additives for ruminants.CrossRef | 1:CAS:528:DC%2BD1cXpsVKrsb0%3D&md5=ce437d0f0cc99d5e5eeb1f6e5cab72e6CAS |

Bryant MP, Small N, Bouma C, Chu H (1958) Bacteroides ruminicola n. sp. and Succinimonas amylolytica; the new genus and species; species of succinic acid-producing anaerobic bacteria of the bovine rumen. Journal of Bacteriology 76, 15–23.

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, Donald DM, 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. Nature Methods 7, 335–336.
QIIME allows analysis of high-throughput community sequencing data.CrossRef | 1:CAS:528:DC%2BC3cXksFalurg%3D&md5=90833d2a4a08cc9373acefde64638d9eCAS | 20383131PubMed |

Danielsson R, Warner-Omazic A, Ramin M, Schnürer A, Griinari M, Dicksved J, Bertilsson J (2014) Effects on enteric methane production and bacterial and archaeal communities by the addition of cashew nut shell extract or glycerol – an in vitro evaluation. Journal of Dairy Science 97, 5729–5741.
Effects on enteric methane production and bacterial and archaeal communities by the addition of cashew nut shell extract or glycerol – an in vitro evaluation.CrossRef | 1:CAS:528:DC%2BC2cXhtFSht73K&md5=00c848645f1cef367728bba963add060CAS | 24996274PubMed |

DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied and Environmental Microbiology 72, 5069–5072.
Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.CrossRef | 1:CAS:528:DC%2BD28XnsVaqtLg%3D&md5=1e1a938d458edf8608634cba388f26a3CAS | 16820507PubMed |

Erwin ES, Marco GJ, Emery EM (1961) Volatile fatty acid analysis of blood and rumen fluid by gas chromatography. Journal of Dairy Science 44, 1768–1771.
Volatile fatty acid analysis of blood and rumen fluid by gas chromatography.CrossRef | 1:CAS:528:DyaF38XhvFKhtQ%3D%3D&md5=33de29aa55d8cf5677d5be563856ef3dCAS |

Fedorah PM, Hrudey SE (1983) A simple apparatus for measuring gas production by methanogenic cultures in serum bottles. Environmental Technology Letters 4, 425–432.
A simple apparatus for measuring gas production by methanogenic cultures in serum bottles.CrossRef |

García-González R, López S, Fernández M, Bodas R, González JS (2008a) Screening the activity of plants and spices for decreasing ruminal methane production in vitro. Animal Feed Science and Technology 147, 36–52.
Screening the activity of plants and spices for decreasing ruminal methane production in vitro.CrossRef |

García-González R, López S, Fernández M, González JS (2008b) Dose–response effects of Rheum officinale root and Frangula alnus bark on ruminal methane production in vitro. Animal Feed Science and Technology 145, 319–334.
Dose–response effects of Rheum officinale root and Frangula alnus bark on ruminal methane production in vitro.CrossRef |

García-González R, González JS, López S (2010) Decrease of ruminal methane production in Rusitec fermenters through the addition of plant material from rhubarb (Rheum spp.) and alder buckthorn (Frangula alnus). Journal of Dairy Science 93, 3755–3763.
Decrease of ruminal methane production in Rusitec fermenters through the addition of plant material from rhubarb (Rheum spp.) and alder buckthorn (Frangula alnus).CrossRef | 20655445PubMed |

García-González R, Francisco JG, Mantecón ÁR, González JS, López S (2012) Effects of rhubarb (Rheum spp.) and frangula (Frangula alnus) on intake, digestibility and ruminal fermentation of different diets and feedstuffs by sheep. Animal Feed Science and Technology 176, 131–139.
Effects of rhubarb (Rheum spp.) and frangula (Frangula alnus) on intake, digestibility and ruminal fermentation of different diets and feedstuffs by sheep.CrossRef |

Hristov AN, Callaway TR, Lee C, Dowd SE (2012) Rumen bacteria, archaeal, and fungal diversity of dairy cows in response to ingestion of lauric or myristic acid. Journal of Animal Science 90, 4449–4457.
Rumen bacteria, archaeal, and fungal diversity of dairy cows in response to ingestion of lauric or myristic acid.CrossRef | 1:CAS:528:DC%2BC3sXns1Skug%3D%3D&md5=6bf220645eafedc63f132eefed68e83dCAS | 22952367PubMed |

IPCC (Intergovernmental Panel on Climate Change) (2007) IPCC Fourth Assessment Report.

Johnson KA, Johnson DE (1995) Methane emissions from cattle. Journal of Animal Science 73, 2483–2492.

Kang SC, Lee CM, Choung ES, Bak JP, Bae JJ, Yoo HS, Kwak JH, Zee OP (2008) Anti-proliferative effects of estrogen receptor-modulating compounds isolated from Rheum palmatum. Archives of Pharmacal Research 31, 722–726.
Anti-proliferative effects of estrogen receptor-modulating compounds isolated from Rheum palmatum.CrossRef | 1:CAS:528:DC%2BD1cXnsVSksr8%3D&md5=cca023fe80afa66314c8a2888d3671dfCAS | 18563353PubMed |

Li ZP, Liu HL, Li GY, Bao K, Aang KY, Xu C, Yang YF, Yang FH, Wright A-DG (2013) Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic Sika deer (Cervus nippon) in China. BMC Microbiology 13, 151–162.
Molecular diversity of rumen bacterial communities from tannin-rich and fiber-rich forage fed domestic Sika deer (Cervus nippon) in China.CrossRef | 1:CAS:528:DC%2BC3sXht1yns7%2FM&md5=d27e554a4f59b1f48c09e0ccc4bffe12CAS | 23834656PubMed |

McIntosh FM, Williams P, Losa R, Wallace RJ, Beever DA, Newbold CJ (2003) Effects of essential oils on ruminal microorganisms and their protein metabolism. Applied and Environmental Microbiology 69, 5011–5014.
Effects of essential oils on ruminal microorganisms and their protein metabolism.CrossRef | 1:CAS:528:DC%2BD3sXmsFWru7o%3D&md5=452d3fda581c752784a95cc2beda75baCAS | 12902303PubMed |

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. British Journal of Nutrition 108, 482–491.
Responses in digestion, rumen fermentation and microbial populations to inhibition of methane formation by a halogenated methane analogue.CrossRef | 1:CAS:528:DC%2BC38XhtFClu7fK&md5=83b9473bdb1c81c275a8f41dc27dae8eCAS | 22059589PubMed |

Miyazawa M, Minamino Y, Kameoka H (1996) Volatile components of the rhizomes of Rheum palmatum L. Flavour and Fragrance Journal 11, 57–60.
Volatile components of the rhizomes of Rheum palmatum L.CrossRef | 1:CAS:528:DyaK28XitVKhtro%3D&md5=835248c44eb2597243fd21ab5304b3efCAS |

Morgavi DP, Rathahao-Paris E, Popova M, Boccard J, Nielson KF, Boudra H (2015) Rumen microbial communities influence metabolic phenotypes in lambs. Fontiers in Microbiology 6, 1060

SAS (2002) ‘SAS user’s guide: statistics.’ (SAS Institute Inc.: Cary, NC)

Stewart CS (1991) The rumen bacteria. In ‘Rumen microbial metabolism and ruminant digestion’. (Ed. JP Jouany) pp. 15–26. (INRA Editions: Paris, France)

Strobel HJ (1992) Vitamin B12-dependent propionate production by the ruminal bacterium Prevotella ruminicola 23. Applied and Environmental Microbiology 58, 2331–2333.

Xiaochen Y, Yinzhuo Y, Kim EB, Bokyung L, Maria LM (2015) Short communication: Effect of milk and milk containing Lactobacillus casei on the intestinal microbiota of mice. Journal of Dairy Science 97, 2049–2055.



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