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Effects of tea saponins on rumen microbiota, rumen fermentation, methane production and growth performance—a review

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Abstract

Reducing methane emission from ruminant animals has implications not only for global environmental protection but also for efficient animal production. Tea saponins (TS) extracted from seeds, leaves or roots of tea plant are pentacyclic triterpenes. They have a lasting antiprotozoal effect, but little effect on the methanogen population in sheep. There was no significant correlation between the protozoa counts and methanogens. The TS decreased methanogen activity. It seems that TS influenced the activity of the methanogens indirectly via the depressed ciliate protozoal population. The TS addition decreased fungal population in the medium containing rumen liquor in in vitro fermentation, but no such effect was observed in the rumen liquor of sheep fed TS. Tea saponins had a minor effect on the pattern of rumen fermentation and hence on nutrient digestion. When added at 3 g/day in diets, TS could improve daily weight gain and feed efficiency in goats. No positive associative effect existed between TS and disodium fumarate or soybean oil on methane suppression. Inclusion of TS in diets may be an effective way for improving feed efficiency in ruminants.

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Abbreviations

DF:

Disodium fumarate

DGGE:

Denaturing gradient gel electrophoresis

DM:

Dry matter

IPCC:

Intergovernmental Panel on Climate Change

MCP:

Microbial protein

mcrA:

Methyl-coenzyme M reductase

SO:

Soybean oil

TS:

Tea saponins

TSDF:

Tea saponins plus disodium fumarate

VFA:

Volatile fatty acids

References

  • Afrose, S., Hossain, M.S., Tsujii, H., 2010. Effect of dietary karaya saponin on serum and egg yolk cholesterol in laying hens, British Poultry Scinece, 51, 797–804

    Article  CAS  Google Scholar 

  • Bauchop, T., 1979. Rumen anaerobic fungi of cattle and sheep, Applied and Environmental Microbiology, 38, 148–158

    PubMed  CAS  Google Scholar 

  • Cheeke, P.R., 2000. Actual and potential applications of Yucca schidigera and Quillaja saponaria saponins in human and animal nutrition, Journal of Animal Science, 77, 1–10

    Google Scholar 

  • Diaz, A., Avendano, M., Escobar, A., 1993. Evaluation of Sapindus saponaria as a defaunating agent and its effects on different rumen digestion parameters, Livestock Research for Rural Development, 5(2), 1–6

    Google Scholar 

  • Finlay, B.J., Esteban, G., Clarke, K.J., Williams, A.G., Embley, T.M., Hirt, R.P., 1994. Some rumen ciliates have endosymbiotic methanogens, FEMS Microbiology Letters, 117, 157–162

    Article  PubMed  CAS  Google Scholar 

  • France, J., Dijkstra, J., 2005. Volatile fatty acid production. In: J. Dijkstra, J.M. Forbes, J. France (eds), Quantitative Aspects of Ruminant Digestion and Metabolism, (CABI Publishing, UK), 157–176

    Chapter  Google Scholar 

  • Goel, G., Makkar, H.P.S., Becker, K., 2008. Changes in microbial community structure, methanogenesis and rumen fermentation in response to saponin-rich fractions from different plant materials, Journal of Applied Microbiology, 105, 770–777

    Article  PubMed  CAS  Google Scholar 

  • Guo, Y.Q., Liu, J.X., Lu, Y., Zhu, W.Y., Denman, S.E., McSweeney, C.S., 2008. Effect of tea saponin on methanogenesis, microbial community structure and expression of mcrA gene, in cultures of rumen microorganisms, Letters in Applied Microbiology, 47, 421–426

    Article  PubMed  CAS  Google Scholar 

  • Guo, X.F., Ruan, L.H., Tan, T., 2009. Effect of theasaponins on the foaming capacity of soy protein, Journal of Henan University of Technology (Natural Science Edition), 30(3), 12–14

    CAS  Google Scholar 

  • Hassan, S.M., Byrd, J.A., Cartwright, A.L., Bailey, C.A., 2010. Hemolytic and antimicrobial activities differ among saponin-rich extracts from Guar, Quillaja, Yucca, and Soybean, Applied Biochemistry and Biotechnology, 162, 1008–1017

    Article  PubMed  CAS  Google Scholar 

  • Hayashi, K., Sagesaka, Y.M., Suzuki, T., Suzuki, Y., 2000. Inactivation of human type A and B influenza viruses by tea-sead saponins, Bioscience, Biotechnology, and Biochemistry, 64, 184–186

    Article  PubMed  CAS  Google Scholar 

  • Headon, D.R., Buggle, K., Nelson, A., Killeen, G., 1991. Glycofractions of the Yucca plant and their role in ammonia control. In: Proceeding of the Alltech’s Seventh Annual Symposium of Biotechnology Feed Industry, (Nicholasville, Kentucky, USA), 95–108

  • Hegarty, R.S., 1999. Reducing rumen methane emissions through elimination of rumen protozoa, Australian Journal of Agricultural Research, 50, 1321–1328

    Article  Google Scholar 

  • Hess, H.D., Kreuzer, M., Diaz, T.E., Lascano, C.E., Carulla, J.E., Soliva, C.R., Machmüller, A., 2003. Saponin rich tropical fruits affect fermentation and methanogensesis in faunated and defaunated rumen fluid, Animal Feed Science and Technology, 109, 79–94

    Article  CAS  Google Scholar 

  • Hu, W.L., Liu, J.X., Ye, J.A., Wu, Y.M., Guo, Y.Q., 2005a. Effect of tea saponin on rumen fermentation in vitro, Animal Feed Science and Technology, 120, 333–339

    Article  CAS  Google Scholar 

  • Hu, W.L., Wu, Y.M., Liu, J.X., Guo, Y.Q., Ye, J.A., 2005b. Tea saponins affect in vitro fermentation and methanogenesis in faunated and defaunated rumen fluid, Journal of Zhejiang University-Science B, 6, 787–792

    Article  PubMed  Google Scholar 

  • Hu, W.L., Liu, J.X., Wu, Y.M., Guo, Y.Q., Ye, J.A., 2006. Effects of tea saponins on in vitro ruminal fermentation and growth performance in growing Boer goat. Archives of Animal Nutrition, 60, 89–97

    Article  PubMed  CAS  Google Scholar 

  • Hussain, I., Cheeke, P.R., 1995. Effect of Yucca scidigera extract on rumen and blood profiles of steers fed concentrate- or roughage-based diets, Animal Feed Science and Technology, 51, 231–242

    Article  CAS  Google Scholar 

  • IPCC (Intergovernmental Panel on Climate Change) (2007) Climate Change 2007. The Scientific Basis, (Cambridge University Press, Cambridge, UK)

    Google Scholar 

  • Ivan, M., Koening, K.M., Teferedegne, B., Newbold, C.J., Entz, T., Rode, L.M., Ibrahim, M., 2004. Effect of the dietrary Enterolobium cyclocarpum foliage on the population dynamics of rumen ciliate protozoa in sheep, Small Ruminant Research, 52, 81–91

    Article  Google Scholar 

  • Johnson, K.A. and Johnson, D.E., 1995. Methane emissions from cattle, Jounal of Animal Science, 73, 2483–2492

    CAS  Google Scholar 

  • Jouany, J.P., 1996. Effect of rumen protozoa on nitrogen utilization by ruminants, Journal of Nutrition, 126, 1335S–1346S

    PubMed  CAS  Google Scholar 

  • Kitagawa, I., Hori, K., Motozawa, T., Murakami, T., Yoshikawa, M., 1998. Structures of new acylated oleanene-type triterpene oligoglycosides, theasaponins E1 and E2, from the seeds of tea plant, Camellia sinensis (L.) O. Kuntze, Chemical and Pharmaceutical Bulletin, 46, 1901–1906

    Article  CAS  Google Scholar 

  • Klita, P.T., Mathison, G.W., Fenton, T.W., Hardin, R.T., 1996. Effects of alfalfa root saponins on digestive function in sheep, Journal of Animal Science, 74, 1144–1156

    PubMed  CAS  Google Scholar 

  • Lila, Z.A., Mohammed, N., Kanda, S., Kamada, T., Itabashi, H., 2003. Effect of sarsaponin on ruminal fermentation with particular reference to methane production in vitro, Journal of Dairy Science, 86, 3330–3336

    Article  PubMed  CAS  Google Scholar 

  • Lopez, S., Valdes, C., Newbold, C.J., Wallace, R.J., 1999. Influence of sodium fumarate addition on rumen fermentation in vitro, British Journal of Nutrition, 81, 59–64

    PubMed  CAS  Google Scholar 

  • Lovett, D.K., Stack, L., Lovell, S., Callan, J., Flynn, B., Hawkins, M., Mara, F.P.O., 2006. Effect of feeding Yucca schidigera extract on performance of lactating dairy cows and ruminal ermentation parameters in steers, Livestock Science, 102, 23–32

    Article  Google Scholar 

  • Machmüller, A., Soliva, C.R., Kreuzer, M., 2003. Methane-suppressing effect of myristic acid in sheep as affected by dietary calcium and forage proportion, British Journal of Nutriton, 90, 529–540

    Article  Google Scholar 

  • Mao, H.L., Wang, J.K., Zhou, Y.Y., Liu J.X., 2010. Effects of addition of tea saponins and soybean oil on methane production, fermentation and microbial population in the rumen of growing lambs, Livestock Science, doi:10.1016/j.livsci.2009.12.011

  • Matsuura, M., 2001. Saponins in garlic as modifiers of the risk of cardiovascular disease, Journal of Nutrition, 131, 1000S–1005S

    PubMed  CAS  Google Scholar 

  • Morikawa, T., Matsuda, H., Li, N., Nakamura, S., Li, X., Yoshikawa, M., 2006. Bioactive saponins and glycosides. XXVI. New Triterpene saponins, theasaponins E10, E11, E12, E13, and G2, from the seeds of tea plant (Camellia sinensis), Heterocycles, 68, 1139–1148

    Article  CAS  Google Scholar 

  • Moss, A.R., Jouany, J.P. and Newbold, J., 2000. Methane production by ruminants: its contribution to global warming, Annales de Zootechnie, 49, 231–253

    Article  CAS  Google Scholar 

  • Mounfort, D.O., Asher, R.A., 1989. Production of xylanase from anaerobic fungus, Neocallimastix frontalis, Applied and Environmental Microbiology, 55, 1016–1022

    Google Scholar 

  • Müller, M., 1993. The hydrogenosome, Journal of General Microbiology, 139, 2879–2889

    PubMed  Google Scholar 

  • Murakami, T., Nakamura, J., Matsuda, H., Yoshikawa, M., 1999. Bioactive saponins and glycosides. XV. Saponin constituents with gastroprotective effect from the seeds of tea plant, Camellia sinensis L. var. assamica PIERRE, cultivated in Sri Lanka: structures of assamsaponins A, B, C, D, and E, Chemical and Pharmaceutical Bulletin, 47, 1759–1764

    Article  CAS  Google Scholar 

  • Murakami, T., Nakamura, J., Kageura, T., Matsuda, H., Yoshikawa, M., 2000. Bioactive saponins and glycosides. XVII. Inhibitory effect on gastric emptying and accelerating effect on gastrointestinal transit of tea saponins: structures of assamsaponins F, G, H, I, and J from the seeds and leaves of the tea plant, Chemical and Pharmaceutical Bulletin, 48, 1720–1725

    Article  CAS  Google Scholar 

  • Nasri, Saïda, Salem, H.Ben, Vasta, V., Abidi, S., Makkar, H.P.S., Priolo, A., 2011. Effect of increasing levels of Quillaja saponaria on digestion, growth and meat quality of Barbarine lamb, Animal Feed Science and Technology, 164, 71–78

    Article  Google Scholar 

  • Newbold, C.J., Lopez, S., Nelson, N., Ouda, J.O., Wallace, R.J., Moss, A.R., 2005. Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro, British Journal of Nutrition, 94, 27–35

    Article  PubMed  CAS  Google Scholar 

  • Nollet, L., Mbanzamihigo, L., Demeyer, D., Verstraete, W., 1998. Effect of the addition of Peptostreptococcus productus ATCC 35244 on reductive acetogenesis in the ruminal ecosystem after inhibition of methanogenesis by cell-free supernatant of Lactobacillus plantarum 80, Animal Feed Science and Technology, 71, 49–66

    Article  CAS  Google Scholar 

  • Oakenfull, D., Sidhu, G., 1990. Could saponins be a useful treatment for hypercholesterolemia? European Journal of Clinical Nutrition, 44, 79–88

    PubMed  CAS  Google Scholar 

  • Owens, F.N., Bergen, W.G., 1983. Nitrogen metabolism of ruminant animals: Historical perspective, current understanding and future Implications, Journal of Animal Science, 57, 498–518

    PubMed  CAS  Google Scholar 

  • Owolabi, O.A., James, D.B., Ibrahim, A.B., Folorunsho, O.F., Bwalla, I., Akanta, F., 2010. Changes in lipid profile of aqueous and ethanolic extract of Blighia sapida in rats, Asian Journal of Medical Sciences, 2, 177–180

    Google Scholar 

  • Rode, L.M., 2000. Maintaining a healthy Rumen – An overview, Advances in Dairy Technology, 12, 101–108

    Google Scholar 

  • Sagesaka, Y.M., Uemura, T., Suzuki, Y., Sugiura, T., Yoshida, M., Yamaguchi, K, Kyuki, K., 1996. Antimicrobial and anti-inflammatory actions of tea-leaf saponin, Yakugaku Zasshi, 116(3), 238–243

    PubMed  CAS  Google Scholar 

  • Santoso, B., Kilmaskossu, A., Sambodoc, P., 2007. Effects of saponin from Biophytum petersianum Klotzsch on ruminal fermentation, microbial protein synthesis and nitrogen utilization in goats, Animal Feed Science and Technology, 137, 58–68

    Article  CAS  Google Scholar 

  • Singer, M.D., Robinson, H.P., Salem, A.Z.M., DePeters, E.J., 2008. Impacts of rumen fluid modified by feeding Yucca schidigera to lactating dairy cows on in vitro gas production of 11 common dairy feedstuffs, as well as animal performance, Animal Feed Science and Technology, 146, 242–258

    Article  Google Scholar 

  • Soliva, C.R., Hess, H.D., Meile, L., 2003. Suppression of ruminal methanogenesis by dietary means: apprent inconsistency between methane release and counts of microbes involved in methanogenesis, Tropical and Subtropical Agroecosystems, 3, 209–213

    Google Scholar 

  • Teferedegne, B., McIntosh, F., Osuji, P.O., Odenyo, A., Wallace, R.J., Newbold, C.J., 1999. Influence of foliage from different accessions of the subtropical leguminous tree, Sesbania sesban on rumen protozoa in Ethiopian and Scottish sheep, Animal Feed Science and Technology, 78, 11–20

    Article  Google Scholar 

  • Thalib, A., Widiawati, Y., Hamid, H., Suherman, D., Sabrani, M., 1996. The effects if saponin from Sapindus rarak fruit on rumen microbes and performance of sheep, Jurnal Ilmu Ternak dan Veteriner (Indonesia), 2, 17–20

    Google Scholar 

  • Tokura, M., Chagan, I., Ushida, K., Kojima, Y., 1999. Phylogenetic study of methanogens associated with rumen ciliates, Current Microbiology, 39, 123–128

    Article  PubMed  CAS  Google Scholar 

  • Ungerfeld, E.M., Rust, S.R., Burnett, R., 2003. Use of some novel alternative electron sinks to inhibit ruminal methanogenesis, Reproduction Nutrition Development, 43, 189–202

    Article  CAS  Google Scholar 

  • Van Soest, P.J., 1994. Nutritional Ecology of the Ruminant, 2nd ed., (Cornell University Press, United States)

    Google Scholar 

  • Vincken, J.P., Heng, L., de Groot, A., Gruppen, H., 2007. Saponins, classification and occurrence in the plant kingdom, Phytochemistry, 68(3), 275–297

    Article  PubMed  CAS  Google Scholar 

  • Vinogradov, E., Egbosimba, E.E., Perry, M.B., Lam, J.S., Forsberg, C.W., 2001. Structural analysis of the carbohydrate components of the outer membrane of the lipopolysaccharide-lacking cellulolytic ruminal bacterium Fibrobacter succinogenes S85, European Journal of Biochemistry, 268, 3566–3576

    Article  PubMed  CAS  Google Scholar 

  • Vogels, G.D., Hoppe, W.F., Stumm, C.K., 1980. Association of methanogenic bacteria with rumen ciliates, Applied and Environmental Microbiology, 40, 608–612

    PubMed  CAS  Google Scholar 

  • Wallace, R.J., McEwan, N.R., McIntosh, F.M., Teferedegne, B., Newbold, C.J., 2002. Natural products as manipulators of rumen fermentation, Asian-Australasian Journal of Animal Sciences, 15(10), 1458–1468

    CAS  Google Scholar 

  • Wang, Y., McAllister, T.A., Newbold, C.J., Rode, L.M., Cheeke, P.R., Cheng, K.-J., 1998. Effect of Yucca schidigera extract on fermentation and degradation of steroidal saponins in the rumen simulation technique (RUSITEC), Animal Feed Science and Technology, 74, 143–153

    Article  CAS  Google Scholar 

  • Wang, Y., McAllister, T.A., Yanke, L.J., Cheeke, P.R., 2000a. Effect of steroidal saponin from Yucca schidigera extract on ruminal microbes, Journal of Applied Microbiology, 88, 887–896

    Article  PubMed  CAS  Google Scholar 

  • Wang, Y.X., McAllister, T.A., Yanke, L.J., Xu, Z.J., Cheeke, P.R. and Cheng, K.-J., 2000b. In vitro effects of steroidal saponins from Yucca Schidiigera extract on rumen microbial protein synthesis and ruminal fermentation, Journal of the Science of Food and Agriculture, 80, 2114–2122

    Article  CAS  Google Scholar 

  • Wang, C.J., Wang, S.P., Zhou, H., 2009. Influences of flavomycin, ropadiar, and saponin on nutrient digestibility, rumen fermentation, and methane emission from sheep, Animal Feed Science and Technology, 148, 157–166

    Article  CAS  Google Scholar 

  • Williams, A.G., Coleman, G.S., Brock, T.D., 1991. The Rumen Protozoa, (Springer-Verlag New York, LLC.)

  • Wina, E., Muetzel, S., Becker, K., 2005a. The impact of saponins or saponin-containing plant materials on ruminant production-a review, Journal of Agricultural and Food Chemistry, 53, 8093–8105

    Article  PubMed  CAS  Google Scholar 

  • Wina, E., Muetzel, S., Hoffman, E., Makkar, H.P.S., Becker, K., 2005b. Saponins containing methanol extract of Sapindus rarak affect munity structure in vitro, Animal Feed Science and Technology, 121, 159–174

    Article  CAS  Google Scholar 

  • Wina, E., Muetzel, S., Becker, K., 2006. The dynamics of major fibrolytic microbes and enzyme activity in the rumen in response to short and long-term feeding of Sapindus rarak saponins, Journal of Applied Microbiology, 100, 114–122

    Article  PubMed  CAS  Google Scholar 

  • Wu, W.T., Chen, J.W., Hsieh, H.J., 2007. Method of emulsifying phytosterol by natural saponin, emulsion prepared thereby and water dispersible phytosterol powder product, United States Patent Application Publication, Appl. No.: 11/179, 472.

  • Yoshikawa, M., Morikawa, T., Li, N., Nagatomo, A., Li, X., Matsuda, H., 2005a. Bioactive Saponins and Glycosides. XXIII. Triterpene Saponins with Gastroprotective Effect from the Seeds of Camellia sinensis-Theasaponins E3, E4, E5, E6, and E7, Chemical and Pharmaceutical Bulletin, 53, 1559–1564

    Article  CAS  Google Scholar 

  • Yoshikawa, M., Morikawa, T., Yamamoto, K., Kato, Y., Nagatomo, A.,Matsuda, H., 2005b. Floratheasaponins A-C, acylated oleanane-type triterpene oligoglycosides with anti-hyperlipidemic activities from flowers of the tea plant (Camellia sinensis), Journal of Natural Products, 68, 1360–1365

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa, M., Morikawa, T., Nakamura, S., Li, N., Li, X., Matsuda, H., 2007. Bioactive Saponins and glycosides. XXV. acylated oleanane-type triterpene saponins from the seeds of tea plant (Camellia sinensis), Chemical and Pharmaceutical Bulletin, 55, 57–63

    Article  CAS  Google Scholar 

  • Yuan, Z.P., Zhang, C.M., Zhou, L., Zou, C.X., Guo, Y.Q., Li, W.T., Liu, J.X. and Wu, Y.M. 2007. Inhibition of methanogenesis by tea saponin and tea saponin plus disodium fumarate in sheep, Journal of Animal and Feed Sciences, 16(Suppl. 2), 560–565

    Google Scholar 

  • Yuan, X.Z., Meng, Y.T., Zeng, G.M., Fang, Y.Y., Shi, J.G., 2008. Evaluation of tea-derived biosurfactant on removing heavy metal ions from dilute wastewater by ion flotation, Colloids and Surfaces: A: Physicochemical and Engineering Aspects, 317, 256–261

    Article  CAS  Google Scholar 

  • Zhang, C.M., Guo, Y.Q., Yuan, Z.P., Wu, Y.M., Wang, J.K., Liu, J.X., Zhu, W.Y., 2008. Effect of octadeca carbon fatty acids on microbial fermentation, methanogensis and microbial flora in vitro, Animal Feed Science and Technology, 146, 259–269

    Article  CAS  Google Scholar 

  • Zhou, Y.Y., Mao, H.L., Jiang, F., Wang, J.K., Liu, J.X., McSweeney, C.S., 2011. Inhibition of rumen methanogenesis by tea saponins with reference to fermentation pattern and microbial communities in Hu sheep, Animal Feed Science and Technology, 166–167, 93–100

    Article  Google Scholar 

  • Zinder, S.H., 1993. Physiological ecology of methanogens. In: J.G.,Ferry (eds), Methanogenesis: Ecology, Physiology, Biochemistry & Genetics. (Chapman & Hall. Inc, New York), 128–206.

    Google Scholar 

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Acknowledgements

The work described in this article was carried out in collaboration with colleagues at the Institute of Dairy Science, College of Animal Sciences, Zhejiang University. We are thankful to Ms. Emma Gagen at CSIRO Livestock Industries, Australia, for critically reading the manuscript and revising the English language. Financial supports from the International Atom Energy Agency (No. 12665/R0) and the National Natural Science Foundation of China (No. 30972105) are acknowledged.

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  1. Institute of Dairy Science, College of Animal Sciences, Zhejiang University, Hangzhou, 310029, People’s Republic of China

    Jia-Kun Wang, Jun-An Ye & Jian-Xin Liu

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Wang, JK., Ye, JA. & Liu, JX. Effects of tea saponins on rumen microbiota, rumen fermentation, methane production and growth performance—a review. Trop Anim Health Prod 44, 697–706 (2012). https://doi.org/10.1007/s11250-011-9960-8

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