Microbial Ecology

, Volume 50, Issue 2, pp 197–205 | Cite as

Bacterial Mechanisms to Overcome Inhibitory Effects of Dietary Tannins

  • Alexandra H. Smith
  • Erwin Zoetendal
  • Roderick I. MackieEmail author


High concentrations of tannins in fodder plants inhibit gastrointestinal bacteria and reduce ruminant performance. Increasing the proportion of tannin-resistant bacteria in the rumen protects ruminants from antinutritional effects. The reason for the protective effect is unclear, but could be elucidated if the mechanism(s) by which tannins inhibit bacteria and the mechanisms of tannin resistance were understood. A review of the literature indicates that the ability of tannins to complex with polymers and minerals is the basis of the inhibitory effect on gastrointestinal bacteria. Mechanisms by which bacteria can overcome inhibition include tannin modification/degradation, dissociation of tannin–substrate complexes, tannin inactivation by high-affinity binders, and membrane modification/repair and metal ion sequestration. Understanding the mechanism of action of tannins and the mechanism(s) bacteria use to overcome the inhibitory effects will allow better management of the rumen ecosystem to reduce the antinutritional effects of tannin-rich fodder plants and thereby improve ruminant production.


Tannin Condensed Tannin Extracellular Polysaccharide Hydrolyzable Tannin Epigallocatechin Gallate 
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.



This research and development was supported in part by funds provided to the International Arid Lands Consortium (IALC) by the USDA Forest Service and by the USDA Cooperative State Research, Education and Extension Service.


  1. 1.
    Akin, DE 1980Attack on lignified grass cell walls by a facultatively anaerobic bacteriumAppl Environ Microbiol40809820PubMedGoogle Scholar
  2. 2.
    Bae, HD, McAllister, TA, Yanke, J, Cheng, K-J, Muir, AD 1993Effects of condensed tannins on endoglucanase activity and filter paper digestion by Fibrobacter succinogenes S85Appl Environ Microbiol5921322138PubMedGoogle Scholar
  3. 3.
    Balmer, SE, Wharton, BA 1991Diet and faecal flora in the newborn: ironArch Dis Child6613901394PubMedCrossRefGoogle Scholar
  4. 4.
    Benoni, G, Cuzzolin, L, Zambreri, D, Donini, M, Soldato, P, Caramazza, I 1993Gastrointestinal effects of single and repeated doses of ferrous sulphate in ratsPharmacol Res277380CrossRefPubMedGoogle Scholar
  5. 5.
    Bhat, TK, Singh, B, Sharma, OP 1998Microbial degradation of tannins—a current perspectiveBiodegradation9343357CrossRefPubMedGoogle Scholar
  6. 6.
    Brooker, JD, O'Donovan, L, Brooker, L, Skene, IK, Sellick, GS 1998Mechanisms of tannin resistance and detoxification in rumen microorganismsBell, CRBrylinsky, MJohnson-Green, P eds. 8th International Symposium on Microbial EcologyAtlantic Canada Society for Microbial EcologyHalifax, Canada409417Google Scholar
  7. 7.
    Brooker, JD, O'Donovan, LA, Brooker, LA, Clarke, K, Blackall, L, Muslera, P 1994Streptococcus caprinus sp. nov., a tannin-resistant ruminal bacterium from feral goatsLett Appl Microbiol18313318Google Scholar
  8. 8.
    Brooker, JD, O'Donovan, LO, Skene, I, Sellick, G 2000Mechanisms of tannin resistance and detoxification in the rumenBrooker, JD eds. Tannins in Livestock and Human Nutrition: Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 921Australian Centre for International Agricultural ResearchAdelaide, Australia117122Google Scholar
  9. 9.
    Chiquette, J, Cheng, K-J, Costerton, JW, Milligan, LP 1988Effect of tannins on the digestibility of two isosynthetic strains of birdsfoot trefoil (Lotus corniculus L.) using in vitro and in sacco techniquesCan J Anim Sci68751760Google Scholar
  10. 10.
    Chung, KT, Lu, Z, Chou, MW 1998Mechanism of inhibition of tannic acid and related compounds on the growth of intestinal bacteriaFood Chem Toxicol3610531060PubMedGoogle Scholar
  11. 11.
    Coates, JD, Cole, KA, Chakraborty, R, O'Connor, SM, Achenbach, LA 2002Diversity and ubiquity of bacteria capable of utilizing humic substances as electron donors for anaerobic respirationAppl Environ Microbiol6824452452CrossRefPubMedGoogle Scholar
  12. 12.
    Dalrymple, BP, Swadling, Y 1997Expression of a Butyrivibrio fibrisolvens E14 gene (cinB) encoding an enzyme with cinnamoyl ester hydrolase activity is negatively regulated by the product of an adjacent gene (cinR)Microbiology14312031210PubMedGoogle Scholar
  13. 13.
    Grbic-Galic, D 1986O-demethylation, dehydroxylation, ring-reduction and cleavage of aromatic substrates by Enterobacteriaceae under anaerobic conditionsJ Appl Bacteriol61491497PubMedGoogle Scholar
  14. 14.
    Gregg, K, Hamdorf, B, Henderson, K, Kopecny, J, Wong, C 1998Genetically modified ruminal bacteria protect sheep from fluoroacetate poisoningAppl Environ Microbiol6434963498PubMedGoogle Scholar
  15. 15.
    Hagerman, AE (2002) Tannin Chemistry: Hagerman Laboratory Methods. Scholar
  16. 16.
    Hashimoto, T, Kumazawa, S, Nanjo, F, Hara, Y, Nakayama, T 1999Interaction of tea catechins with lipid bilayers investigated with liposome systemsBiosci Biotechnol Biochem6322522255PubMedGoogle Scholar
  17. 17.
    Haslam, E 1996Natural polyphenols (vegetable tannins) as drugs: possible modes of actionJ Nat Prod59205215CrossRefPubMedGoogle Scholar
  18. 18.
    Ikigai, H, Nakae, T, Hara, Y, Shimamura, T 1993Bactericidal catechins damage the lipid bilayerBiochim Biophys Acta1147132136PubMedGoogle Scholar
  19. 19.
    Jones, GA, McAllister, TA, Muir, AD, Cheng, KG 1994Effects of sainfoin (Onobrychis viciifolia scop.) condensed tannins on growth and proteolysis by four strains of ruminal bacteriaAppl Environ Microbiol6013741378PubMedGoogle Scholar
  20. 20.
    Kitano, K, Nam, KY, Kimura, S, Fujiki, H, Imanishi, Y 1997Sealing effects of (−)-epigallocatechin gallate on protein kinase C and protein phosphatase 2ABiophys Chem65157164CrossRefPubMedGoogle Scholar
  21. 21.
    Krumholz, LR, Bryant, MP 1985Clostridium pfennigii sp. nov. uses methoxyl groups of monobenzoids and produces butyrateInt J Syst Bacteriol35454456CrossRefGoogle Scholar
  22. 22.
    Krumholz, LR, Bryant, MP 1986Eubacterium oxidoreducens sp. nov. requiring H2 or formate to degrade gallate, pyrogallol, phloroglucinol and quercetinArch Microbiol144814CrossRefGoogle Scholar
  23. 23.
    Krumholz, LR, Bryant, MP 1986Syntrophococcus sucromutans sp. nov. gen. nov. uses carbohydrates as electron donors and formate, methoxymonobenzenoids or Methanobrevibacter as electron acceptor systemsArch Microbiol143313318CrossRefGoogle Scholar
  24. 24.
    Krumholz, LR, Crawford, RL, Hemling, ME, Bryant, MP 1987Metabolism of gallate and phloroglucinol in Eubacterium oxidoreducens via 3-hydroxy-5-oxohexanoateJ Bacteriol16918861890PubMedGoogle Scholar
  25. 25.
    Makkar, HPS, Becker, K 1995Degradation of condensed tannins by rumen microbes exposed to quebracho tannins (QT) in rumen simulation technique (RUSITEC) and effects of QT on fermentative processes in the RUSITECJ Sci Food Agric69495500Google Scholar
  26. 26.
    Makkar, HPS, Blümmel, M, Becker, K 1995In vitro effects of and interactions between tannins and saponins and fate of tannins in the rumenJ Sci Food Agric69481493Google Scholar
  27. 27.
    Mangan, JL 1988Nutritional effects of tannins in animal feedsNutr Res Rev1209231CrossRefPubMedGoogle Scholar
  28. 28.
    McDonald, M, Mila, I, Scalbert, A 1996Precipitation of metal ions by plant polyphenols: optimal conditions and origin of precipitationJ Agric Food Chem44599606CrossRefGoogle Scholar
  29. 29.
    McMahon, LR, McAllister, TA, Berg, BP, Majak, W, Acharya, SN, Popp, JD, Coulman, BE, Wang, Y, Cheng, K-J 2000A review of the effects of forage condensed tannins on ruminal fermentation and bloat in grazing cattleCan J Plant Sci80469485Google Scholar
  30. 30.
    McSweeney, CS, Dulieu, A, Webb, RI, Dot, T, Blackall, LL 1999Isolation and characterization of a Clostridium sp. with cinnamoyl esterase activity and unusual cell envelop ultrastructureArch Microbiol172139149CrossRefPubMedGoogle Scholar
  31. 31.
    McSweeney, CS, Palmer, B, Bunch, R, Krause, DO 1999Isolation and characterization of proteolytic ruminal bacteria from sheep and goats fed the tannin-containing shrub legume Calliandra calothyrsus Appl Environ Microbiol6530753083PubMedGoogle Scholar
  32. 32.
    McSweeney, CS, Palmer, B, Krause, DO 2000Rumen microbial ecology and physiology in sheep and goats fed a tannin-containing dietBrooker, JD eds. Tannins in Livestock and Human Nutrition: Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 92Australian Centre for International Agricultural ResearchAdelaide, Australia140145Google Scholar
  33. 33.
    McSweeney, CS, Palmer, B, McNeill, DM, Krause, DO 2001Microbial interactions with tannins: nutritional consequences for ruminantsAnim Feed Sci Technol918393CrossRefGoogle Scholar
  34. 34.
    Mila, I, Scalbert, A, Expert, D 1996Iron withholding by plant polyphenols and resistance to pathogens and rotsPhytochemistry4215511555CrossRefGoogle Scholar
  35. 35.
    Miller, SM, Brooker, JD, Blackall, LL 1995A feral goat rumen fluid inoculum improves nitrogen retention in sheep consuming a mulga (Acacia aneura) dietAust J Agric Res4615451553CrossRefGoogle Scholar
  36. 36.
    Miller, SM, Brooker, JD, Philips, A, Blackall, LL 1996Streptococcus caprinus is ineffective as a rumen inoculum to improve digestion of mulga (Acacia aneura) by sheepAust J Agric Res4713231331CrossRefGoogle Scholar
  37. 37.
    Miller, SM, Klieve, AV, Plumb, JJ, Blackall, LL 1997An in vitro cultured rumen inoculum improves nitrogen digestion in mulga-fed sheepAust J Agric Res48403409Google Scholar
  38. 38.
    Min, BR, Attwood, GT, Reilly, K, Sun, W, Peters, JS, Barry, TN, McNabb, WC 2002Lotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheepCan J Microbiol48911921CrossRefPubMedGoogle Scholar
  39. 39.
    Molan, AL, Attwood, GT, Min, BR, McNabb, WC 2001The effect of condensed tannins from Lotus pedunculatus and Lotus corniculatus on the growth of proteolytic rumen bacteria invitro and their possible mode of actionCan J Microbiol47626633CrossRefPubMedGoogle Scholar
  40. 40.
    Mole, S, Butler, LG, Iason, G 1990Defense against dietary tannin in herbivores: a survey for proline rich salivary proteins in mammalsBiochem Syst Ecol18287293Google Scholar
  41. 41.
    Molina, DO, Pell, AN, Hogue, DE 1999Effects of ruminal inoculations with tannin-tolerant bacteria on fibre and nitrogen digestibility of lambs fed a high condensed tannin dietAnim Feed Sci Technol81669680CrossRefGoogle Scholar
  42. 42.
    Mueller-Harvey, I 2001Analysis of hydrolysable tanninsAnim Feed Sci Technol91320CrossRefGoogle Scholar
  43. 43.
    Nelson, KE, Pell, AN, Schofield, P, Zinder, S 1995Isolation and characterization of an anaerobic ruminal bacterium capable ofdegrading hydrolyzable tanninsAppl Environ Microbiol6132933298PubMedGoogle Scholar
  44. 44.
    Nelson, KE, Thonney, ML, Woolston, TK, Zinder, SH, Pell, AN 1998Phenotypic and phylogenetic characterization of ruminal tannin-tolerant bacteriaAppl Environ Microbiol6438243830PubMedGoogle Scholar
  45. 45.
    Nemoto, K, Osawa, R, Hirota, K, Ono, T, Miyake, Y 1995An investigation of Gram-negative tannin–protein complex degrading bacteria in fecal flora of various mammalsJ Vet Med Sci57921926PubMedGoogle Scholar
  46. 46.
    O'Donovan, L, Brooker, JD 2001Effect of hydrolysable and condensed tannins on growth, morphology and metabolism of Streptococcus gallolyticus (S. caprinus) and Streptococcus bovis Microbiology14710251033PubMedGoogle Scholar
  47. 47.
    Odenyo, AA, Bishop, R, Asefa, G, Jamnadass, R, Odongo, D, Osuji, P 2001Characterization of tannin-tolerant bacterial isolates from East African ruminantsAnaerobe7515CrossRefGoogle Scholar
  48. 48.
    Odenyo, AA, Osuji, PO 1998Tannin-tolerant ruminal bacteria from East African ruminantsCan J Microbiol44905909CrossRefPubMedGoogle Scholar
  49. 49.
    Odenyo, AA, Osuji, PO, Karanfil, O, Adinew, K 1997Microbiological evaluation of Acacia angustissima as a protein supplement for sheepAnim Feed Sci Technol6599112CrossRefGoogle Scholar
  50. 50.
    Osawa, R 1990Formation of a clear zone on tannin-treated brain heart infusion agar by a Streptococcus sp. isolated from feces of koalasAppl Environ Microbiol56829831PubMedGoogle Scholar
  51. 51.
    Osawa, R, Kuroiso, K, Goto, S, Shimizu, A 2000Isolation of tannin-degrading Lactobacilli from humans and fermented foodsAppl Environ Microbiol6630933097CrossRefPubMedGoogle Scholar
  52. 52.
    Osawa, R, Rainey, F, Fujisawa, T, Lang, E, Busse, HJ, Walsh, TP, Stackebrandt, E 1995Lonepinella koalarum gen. nov., sp. nov., a new tannin–protein complex degrading bacteriumSyst Appl Microbiol18368373Google Scholar
  53. 53.
    Osawa, RO 1992Tannin–protein complex-degrading enterobacteria isolated from the alimentary tracts of koalas and a selective medium for their enumerationAppl Environ Microbiol5817541759PubMedGoogle Scholar
  54. 54.
    Osawa, RO, Fujisowa, T, Sly, LI 1995Streptococcus gallolyticus sp. nov. gallate degrading organisms formerly assigned to Streptococcus bovisSyst Appl Microbiol187479Google Scholar
  55. 55.
    Pell, AN, Woolston, TK, Nelson, KE, Schofield, P 2000Tannins: biological activity and bacterial toleranceBrooker, JD eds. Tannins in Livestock and Human Nutrition, Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 921Australian Centre for International Agricultural ResearchAdelaide, Australia121126Google Scholar
  56. 56.
    Perez-Maldonado, RA, Norton, BW 1996Digestion of 14C-labelled condensed tannins from Desmodium intortum in sheep and goatsBr J Nutr76501513PubMedGoogle Scholar
  57. 57.
    Pinkart, H, White, D 1997Phosolipid biosynthesis and solvent tolerance in Pseudomonas putida strainsJ Bacteriol17942194226PubMedGoogle Scholar
  58. 58.
    Ramos, JL, Duque, E, Rodriguez-Herva, JJ, Godoy, P, Haidour, A, Reyes, F, Fernandez-Barrero, A 1997Mechanisms for solvent tolerance in bacteriaJ Biol Chem27238873890PubMedGoogle Scholar
  59. 59.
    Ratty, AK, Sunamoto, J, Das, NP 1988Interaction of flavonoids with 1,1-diphenyl-2-picrylhydrazyl free radical, liposomal membranes and soybean lipoxygenase-1Biochem Pharmacol37989995CrossRefPubMedGoogle Scholar
  60. 60.
    Rozes, N, Peres, C 1998Effects of phenolic compounds on the growth and the fatty acid composition of Lactobacillus plantarum Appl Microbiol Biotechnol49108111Google Scholar
  61. 61.
    Sakanaka, S, Aizawa, M, Kim, M, Yamamoto, T 1996Inhibitory effects of green tea polyphenols on growth and cellular adherence of an oral bacterium, Porphyromonas gingivalis Biosci Biotechnol Biochem60745749PubMedGoogle Scholar
  62. 62.
    Scalbert, A 1991Antimicrobial properties of tanninsPhytochemistry3038753883CrossRefGoogle Scholar
  63. 63.
    Schneider, H, Blaut, M 2000Anaerobic degradation of flavonoids by Eubacterium ramulus Arch Microbiol1737175CrossRefPubMedGoogle Scholar
  64. 64.
    Schofield, P, Mbugua, DM, Pell, AN 2001Analysis of condensed tannins: a reviewAnim Feed Sci Technol912140CrossRefGoogle Scholar
  65. 65.
    Sebat, JL, Paszczynski, AJ, Cortese, MS, Crawford, RL 2001Antimicrobial properties of pyridine-2,6-dithiocarboxylic acid, a metal chelator produced by Pseudomonas sppAppl Environ Microbiol6739343942CrossRefPubMedGoogle Scholar
  66. 66.
    Silanikove, N, Gilboa, N, Nitsan, Z 2001Effect of polyethylene glycol on rumen volume and retention time of liquid and particulate matter along the digestive tract in goats fed tannin-rich carob leaves (Ceratonia siliqua)Small Rumin Res409599CrossRefPubMedGoogle Scholar
  67. 67.
    Sly, LI, Cahill, MM, Osawa, RO, Fujisawa, T 1997The tannin-degrading species Streptococcus gallolyticus and Streptococcus caprinus are subjective synonymsInt J Syst Bacteriol47893894PubMedGoogle Scholar
  68. 68.
    Smith, AH, Imlay, J, Mackie, RI 2003Increasing the oxidative stress response allows Escherichia coli to overcome inhibitory effects of condensed tanninsAppl Environ Microbiol6934063411PubMedGoogle Scholar
  69. 69.
    Smith, AH, Mackie, RI 2004The effect of condensed tannins on bacterial diversity and metabolic activity in the rat gastrointestinal tractAppl Environ Microbiol7011041115PubMedGoogle Scholar
  70. 70.
    Smith, AH, Odenyo, AA, Osuji, PO, Wallig, MA, Kandil, FE, Seigler, DS, Mackie, RI 2001Evaluation of toxicity of Acacia angustissima in a rat bioassayAnim Feed Sci Technol914157CrossRefGoogle Scholar
  71. 71.
    Spencer, CM, Cai, Y, Martin, R, Gaffney, SH, Goulding, PN, Magnolato, D, Lilley, TH, Haslam, E 1988Polyphenol complexation—some thoughts and observationsPhytochemistry2723972409Google Scholar
  72. 72.
    Sreerangaraju, G, Krishnamoorthy, U, Kailas, MM 2000Evaluation of Bengal gram (Cicer arietinum) husk a source of tannin and its interference in rumen and post-rumen nutrient digestion in sheepAnim Feed Sci Technol85131138CrossRefGoogle Scholar
  73. 73.
    Terao, J, Piskula, M, Yao, Q 1994Protective effect of epicatechin, epicatechin gallate, and quercetin on lipid peroxidation in phospholipid bilayersArch Biochem Biophys308278284CrossRefPubMedGoogle Scholar
  74. 74.
    Terrill, TH, Waghorn, GC, Woolley, DJ, McNabb, WC, Barry, TN 1994Assay and digestion of 14C-labelled condensed tannins in the gastrointestinal tract of sheepBr J Nutr72467477PubMedCrossRefGoogle Scholar
  75. 75.
    Tompkins, GR, O'Dell, NL, Bryson, IT, Pennington, CB 2001The effects of dietary ferric iron and iron deprivation on the bacterial composition of the mouse intestineCurr Microbiol433842CrossRefPubMedGoogle Scholar
  76. 76.
    Tsuchiya, H 1999Effects of green tea catechins on membrane fluidityPharmacology593444CrossRefPubMedGoogle Scholar
  77. 77.
    Winter, J, Moore, LH, Dowell, VR,Jr, Bokkenheuser, VD 1989C-ring cleavage of flavonoids by human intestinal bacteriaAppl Environ Microbiol5512031208PubMedGoogle Scholar
  78. 78.
    Wiryawan, KG, Tangendjaja, B, Suryahadi, A 2000Tannin degrading bacteria from Indonesian ruminantsBrooker, JD eds. Tannins in Livestock and Human Nutrition: Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 921Australian Centre for International Agricultural ResearchAdelaide, Australia123126Google Scholar
  79. 79.
    Zoetendal, EG, Smith, AH, Sundset, MA, Akan, DH, Mackie, RI (2004) Characterization of the mechanisms of tannin resistance in Escherichia coli by transcriptional profiling. ASM Annual Meeting Abstracts N-143, New Orleans, LAGoogle Scholar
  80. 80.
    Zoetendal, EG, Smith, AH, Sundset, MA, Akan, DH, Mackie, RI (2004) Studying the mechanisms of tannin resistance in Escherichia coli by transcriptional profiling. ISME-10 Abstracts, pp 126, Cancun, MexicoGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Alexandra H. Smith
    • 1
  • Erwin Zoetendal
    • 2
  • Roderick I. Mackie
    • 3
    • 4
    Email author
  1. 1.Department of MicrobiologyUniversity of TexasDallasUSA
  2. 2.Laboratory of MicrobiologyWageningen UniversityWageningenThe Netherlands
  3. 3.Department of Animal SciencesUniversity of IllinoisUrbanaUSA
  4. 4.Division of Nutritional SciencesUniversity of IllinoisUrbanaUSA

Personalised recommendations