Skip to main content

Advertisement

SpringerLink
Log in

Bacterial Mechanisms to Overcome Inhibitory Effects of Dietary Tannins

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. DE Akin (1980) ArticleTitleAttack on lignified grass cell walls by a facultatively anaerobic bacterium Appl Environ Microbiol 40 809–820 Occurrence Handle1:CAS:528:DyaL3cXmtlGjsLc%3D Occurrence Handle16345651

    CAS  PubMed  Google Scholar 

  2. HD Bae TA McAllister J Yanke K-J Cheng AD Muir (1993) ArticleTitleEffects of condensed tannins on endoglucanase activity and filter paper digestion by Fibrobacter succinogenes S85 Appl Environ Microbiol 59 2132–2138 Occurrence Handle1:CAS:528:DyaK3sXlsFGru74%3D Occurrence Handle16348990

    CAS  PubMed  Google Scholar 

  3. SE Balmer BA Wharton (1991) ArticleTitleDiet and faecal flora in the newborn: iron Arch Dis Child 66 1390–1394 Occurrence Handle1776883 Occurrence Handle1:STN:280:DyaK387jsVSkug%3D%3D Occurrence Handle10.1136/adc.66.12.1390

    Article  PubMed  CAS  Google Scholar 

  4. G Benoni L Cuzzolin D Zambreri M Donini P Soldato ParticleDel I Caramazza (1993) ArticleTitleGastrointestinal effects of single and repeated doses of ferrous sulphate in rats Pharmacol Res 27 73–80 Occurrence Handle10.1006/phrs.1993.1007 Occurrence Handle8456060 Occurrence Handle1:CAS:528:DyaK3sXktVSlu7w%3D

    Article  PubMed  CAS  Google Scholar 

  5. TK Bhat B Singh OP Sharma (1998) ArticleTitleMicrobial degradation of tannins—a current perspective Biodegradation 9 343–357 Occurrence Handle10.1023/A:1008397506963 Occurrence Handle10192896 Occurrence Handle1:CAS:528:DyaK1MXisVKhsbk%3D

    Article  PubMed  CAS  Google Scholar 

  6. JD Brooker L O'Donovan L Brooker IK Skene GS Sellick (1998) Mechanisms of tannin resistance and detoxification in rumen microorganisms CR Bell M Brylinsky P Johnson-Green (Eds) 8th International Symposium on Microbial Ecology Atlantic Canada Society for Microbial Ecology Halifax, Canada 409–417

    Google Scholar 

  7. JD Brooker LA O'Donovan LA Brooker K Clarke L Blackall P Muslera (1994) ArticleTitleStreptococcus caprinus sp. nov., a tannin-resistant ruminal bacterium from feral goats Lett Appl Microbiol 18 313–318 Occurrence Handle1:CAS:528:DyaK2MXjslymug%3D%3D

    CAS  Google Scholar 

  8. JD Brooker LO O'Donovan I Skene G Sellick (2000) Mechanisms of tannin resistance and detoxification in the rumen JD Brooker (Eds) Tannins in Livestock and Human Nutrition: Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 92 EditionNumber1 Australian Centre for International Agricultural Research Adelaide, Australia 117–122

    Google Scholar 

  9. J Chiquette K-J Cheng JW Costerton LP Milligan (1988) ArticleTitleEffect of tannins on the digestibility of two isosynthetic strains of birdsfoot trefoil (Lotus corniculus L.) using in vitro and in sacco techniques Can J Anim Sci 68 751–760

    Google Scholar 

  10. KT Chung Z Lu MW Chou (1998) ArticleTitleMechanism of inhibition of tannic acid and related compounds on the growth of intestinal bacteria Food Chem Toxicol 36 1053–1060 Occurrence Handle9862646 Occurrence Handle1:CAS:528:DyaK1MXitVyh

    PubMed  CAS  Google Scholar 

  11. JD Coates KA Cole R Chakraborty SM O'Connor LA Achenbach (2002) ArticleTitleDiversity and ubiquity of bacteria capable of utilizing humic substances as electron donors for anaerobic respiration Appl Environ Microbiol 68 2445–2452 Occurrence Handle10.1128/AEM.68.5.2445-2452.2002 Occurrence Handle11976120 Occurrence Handle1:CAS:528:DC%2BD38XjsFGqtb8%3D

    Article  PubMed  CAS  Google Scholar 

  12. BP Dalrymple Y Swadling (1997) ArticleTitleExpression 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) Microbiology 143 1203–1210 Occurrence Handle9141683 Occurrence Handle1:CAS:528:DyaK2sXjtVWqsLY%3D

    PubMed  CAS  Google Scholar 

  13. D Grbic-Galic (1986) ArticleTitleO-demethylation, dehydroxylation, ring-reduction and cleavage of aromatic substrates by Enterobacteriaceae under anaerobic conditions J Appl Bacteriol 61 491–497 Occurrence Handle3549663 Occurrence Handle1:CAS:528:DyaL2sXhsFakt74%3D

    PubMed  CAS  Google Scholar 

  14. K Gregg B Hamdorf K Henderson J Kopecny C Wong (1998) ArticleTitleGenetically modified ruminal bacteria protect sheep from fluoroacetate poisoning Appl Environ Microbiol 64 3496–3498 Occurrence Handle9726903 Occurrence Handle1:CAS:528:DyaK1cXmtVajtb4%3D

    PubMed  CAS  Google Scholar 

  15. Hagerman, AE (2002) Tannin Chemistry: Hagerman Laboratory Methods. http://www.users.muohio.edu/hagermae/

  16. T Hashimoto S Kumazawa F Nanjo Y Hara T Nakayama (1999) ArticleTitleInteraction of tea catechins with lipid bilayers investigated with liposome systems Biosci Biotechnol Biochem 63 2252–2255 Occurrence Handle10664864 Occurrence Handle1:CAS:528:DC%2BD3cXlsFKqsg%3D%3D

    PubMed  CAS  Google Scholar 

  17. E Haslam (1996) ArticleTitleNatural polyphenols (vegetable tannins) as drugs: possible modes of action J Nat Prod 59 205–215 Occurrence Handle10.1021/np960040+ Occurrence Handle8991956 Occurrence Handle1:CAS:528:DyaK28XnvFeiuw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  18. H Ikigai T Nakae Y Hara T Shimamura (1993) ArticleTitleBactericidal catechins damage the lipid bilayer Biochim Biophys Acta 1147 132–136 Occurrence Handle8466924 Occurrence Handle1:CAS:528:DyaK3sXitlSjtrg%3D

    PubMed  CAS  Google Scholar 

  19. GA Jones TA McAllister AD Muir KG Cheng (1994) ArticleTitleEffects of sainfoin (Onobrychis viciifolia scop.) condensed tannins on growth and proteolysis by four strains of ruminal bacteria Appl Environ Microbiol 60 1374–1378 Occurrence Handle1:CAS:528:DyaK2cXis1egur8%3D Occurrence Handle16349244

    CAS  PubMed  Google Scholar 

  20. K Kitano KY Nam S Kimura H Fujiki Y Imanishi (1997) ArticleTitleSealing effects of (−)-epigallocatechin gallate on protein kinase C and protein phosphatase 2A Biophys Chem 65 157–164 Occurrence Handle10.1016/S0301-4622(96)02254-5 Occurrence Handle9175270 Occurrence Handle1:CAS:528:DyaK2sXivV2ntLg%3D

    Article  PubMed  CAS  Google Scholar 

  21. LR Krumholz MP Bryant (1985) ArticleTitleClostridium pfennigii sp. nov. uses methoxyl groups of monobenzoids and produces butyrate Int J Syst Bacteriol 35 454–456 Occurrence Handle1:CAS:528:DyaL2MXmtFWjs78%3D Occurrence Handle10.1099/00207713-35-4-454

    Article  CAS  Google Scholar 

  22. LR Krumholz MP Bryant (1986) ArticleTitleEubacterium oxidoreducens sp. nov. requiring H2 or formate to degrade gallate, pyrogallol, phloroglucinol and quercetin Arch Microbiol 144 8–14 Occurrence Handle10.1007/BF00454948 Occurrence Handle1:CAS:528:DyaL28XhsVGhtLs%3D

    Article  CAS  Google Scholar 

  23. LR Krumholz MP Bryant (1986) ArticleTitleSyntrophococcus sucromutans sp. nov. gen. nov. uses carbohydrates as electron donors and formate, methoxymonobenzenoids or Methanobrevibacter as electron acceptor systems Arch Microbiol 143 313–318 Occurrence Handle10.1007/BF00412795 Occurrence Handle1:CAS:528:DyaL28XosFWrsA%3D%3D

    Article  CAS  Google Scholar 

  24. LR Krumholz RL Crawford ME Hemling MP Bryant (1987) ArticleTitleMetabolism of gallate and phloroglucinol in Eubacterium oxidoreducens via 3-hydroxy-5-oxohexanoate J Bacteriol 169 1886–1890 Occurrence Handle3571153 Occurrence Handle1:CAS:528:DyaL2sXksFGnt7s%3D

    PubMed  CAS  Google Scholar 

  25. HPS Makkar K Becker (1995) ArticleTitleDegradation 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 RUSITEC J Sci Food Agric 69 495–500 Occurrence Handle1:CAS:528:DyaK2MXpvFegtb0%3D

    CAS  Google Scholar 

  26. HPS Makkar M Blümmel K Becker (1995) ArticleTitleIn vitro effects of and interactions between tannins and saponins and fate of tannins in the rumen J Sci Food Agric 69 481–493 Occurrence Handle1:CAS:528:DyaK2MXpvFegtbw%3D

    CAS  Google Scholar 

  27. JL Mangan (1988) ArticleTitleNutritional effects of tannins in animal feeds Nutr Res Rev 1 209–231 Occurrence Handle10.1079/NRR19880015 Occurrence Handle1:CAS:528:DyaL1MXktVGqtL4%3D Occurrence Handle19094367

    Article  CAS  PubMed  Google Scholar 

  28. M McDonald I Mila A Scalbert (1996) ArticleTitlePrecipitation of metal ions by plant polyphenols: optimal conditions and origin of precipitation J Agric Food Chem 44 599–606 Occurrence Handle10.1021/jf950459q Occurrence Handle1:CAS:528:DyaK28XmsV2itQ%3D%3D

    Article  CAS  Google Scholar 

  29. LR McMahon TA McAllister BP Berg W Majak SN Acharya JD Popp BE Coulman Y Wang K-J Cheng (2000) ArticleTitleA review of the effects of forage condensed tannins on ruminal fermentation and bloat in grazing cattle Can J Plant Sci 80 469–485 Occurrence Handle1:CAS:528:DC%2BD3cXmvVWmsLg%3D

    CAS  Google Scholar 

  30. CS McSweeney A Dulieu RI Webb T Dot ParticleDel LL Blackall (1999) ArticleTitleIsolation and characterization of a Clostridium sp. with cinnamoyl esterase activity and unusual cell envelop ultrastructure Arch Microbiol 172 139–149 Occurrence Handle10.1007/s002030050753 Occurrence Handle10460884 Occurrence Handle1:CAS:528:DyaK1MXmt1Gqsbk%3D

    Article  PubMed  CAS  Google Scholar 

  31. CS McSweeney B Palmer R Bunch DO Krause (1999) ArticleTitleIsolation and characterization of proteolytic ruminal bacteria from sheep and goats fed the tannin-containing shrub legume Calliandra calothyrsus Appl Environ Microbiol 65 3075–3083 Occurrence Handle10388706 Occurrence Handle1:CAS:528:DyaK1MXktlemtbg%3D

    PubMed  CAS  Google Scholar 

  32. CS McSweeney B Palmer DO Krause (2000) Rumen microbial ecology and physiology in sheep and goats fed a tannin-containing diet JD Brooker (Eds) Tannins in Livestock and Human Nutrition: Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 92 Australian Centre for International Agricultural Research Adelaide, Australia 140–145

    Google Scholar 

  33. CS McSweeney B Palmer DM McNeill DO Krause (2001) ArticleTitleMicrobial interactions with tannins: nutritional consequences for ruminants Anim Feed Sci Technol 91 83–93 Occurrence Handle10.1016/S0377-8401(01)00232-2 Occurrence Handle1:CAS:528:DC%2BD3MXjslSms7Y%3D

    Article  CAS  Google Scholar 

  34. I Mila A Scalbert D Expert (1996) ArticleTitleIron withholding by plant polyphenols and resistance to pathogens and rots Phytochemistry 42 1551–1555 Occurrence Handle10.1016/0031-9422(96)00174-4 Occurrence Handle1:CAS:528:DyaK28XkvVKktrc%3D

    Article  CAS  Google Scholar 

  35. SM Miller JD Brooker LL Blackall (1995) ArticleTitleA feral goat rumen fluid inoculum improves nitrogen retention in sheep consuming a mulga (Acacia aneura) diet Aust J Agric Res 46 1545–1553 Occurrence Handle10.1071/AR9951545 Occurrence Handle1:CAS:528:DyaK28XhtFylsLc%3D

    Article  CAS  Google Scholar 

  36. SM Miller JD Brooker A Philips LL Blackall (1996) ArticleTitleStreptococcus caprinus is ineffective as a rumen inoculum to improve digestion of mulga (Acacia aneura) by sheep Aust J Agric Res 47 1323–1331 Occurrence Handle10.1071/AR9961323

    Article  Google Scholar 

  37. SM Miller AV Klieve JJ Plumb LL Blackall (1997) ArticleTitleAn in vitro cultured rumen inoculum improves nitrogen digestion in mulga-fed sheep Aust J Agric Res 48 403–409

    Google Scholar 

  38. BR Min GT Attwood K Reilly W Sun JS Peters TN Barry WC McNabb (2002) ArticleTitleLotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheep Can J Microbiol 48 911–921 Occurrence Handle10.1139/w02-087 Occurrence Handle12489781 Occurrence Handle1:CAS:528:DC%2BD38XpsFOqurk%3D

    Article  PubMed  CAS  Google Scholar 

  39. AL Molan GT Attwood BR Min WC McNabb (2001) ArticleTitleThe effect of condensed tannins from Lotus pedunculatus and Lotus corniculatus on the growth of proteolytic rumen bacteria invitro and their possible mode of action Can J Microbiol 47 626–633 Occurrence Handle10.1139/cjm-47-7-626 Occurrence Handle11547882 Occurrence Handle1:CAS:528:DC%2BD3MXms1SntLg%3D

    Article  PubMed  CAS  Google Scholar 

  40. S Mole LG Butler G Iason (1990) ArticleTitleDefense against dietary tannin in herbivores: a survey for proline rich salivary proteins in mammals Biochem Syst Ecol 18 287–293 Occurrence Handle1:CAS:528:DyaK3cXlsFWjs7Y%3D

    CAS  Google Scholar 

  41. DO Molina AN Pell DE Hogue (1999) ArticleTitleEffects of ruminal inoculations with tannin-tolerant bacteria on fibre and nitrogen digestibility of lambs fed a high condensed tannin diet Anim Feed Sci Technol 81 669–680 Occurrence Handle10.1016/S0377-8401(99)00083-8

    Article  Google Scholar 

  42. I Mueller-Harvey (2001) ArticleTitleAnalysis of hydrolysable tannins Anim Feed Sci Technol 91 3–20 Occurrence Handle10.1016/S0377-8401(01)00227-9 Occurrence Handle1:CAS:528:DC%2BD3MXjslSmsrY%3D

    Article  CAS  Google Scholar 

  43. KE Nelson AN Pell P Schofield S Zinder (1995) ArticleTitleIsolation and characterization of an anaerobic ruminal bacterium capable ofdegrading hydrolyzable tannins Appl Environ Microbiol 61 3293–3298 Occurrence Handle7574640 Occurrence Handle1:CAS:528:DyaK2MXnvVyisb4%3D

    PubMed  CAS  Google Scholar 

  44. KE Nelson ML Thonney TK Woolston SH Zinder AN Pell (1998) ArticleTitlePhenotypic and phylogenetic characterization of ruminal tannin-tolerant bacteria Appl Environ Microbiol 64 3824–3830 Occurrence Handle9758806 Occurrence Handle1:CAS:528:DyaK1cXms1entLo%3D

    PubMed  CAS  Google Scholar 

  45. K Nemoto R Osawa K Hirota T Ono Y Miyake (1995) ArticleTitleAn investigation of Gram-negative tannin–protein complex degrading bacteria in fecal flora of various mammals J Vet Med Sci 57 921–926 Occurrence Handle8593303 Occurrence Handle1:STN:280:DyaK287lsFylsg%3D%3D

    PubMed  CAS  Google Scholar 

  46. L O'Donovan JD Brooker (2001) ArticleTitleEffect of hydrolysable and condensed tannins on growth, morphology and metabolism of Streptococcus gallolyticus (S. caprinus) and Streptococcus bovis Microbiology 147 1025–1033 Occurrence Handle11283298

    PubMed  Google Scholar 

  47. AA Odenyo R Bishop G Asefa R Jamnadass D Odongo P Osuji (2001) ArticleTitleCharacterization of tannin-tolerant bacterial isolates from East African ruminants Anaerobe 7 5–15 Occurrence Handle10.1006/anae.2000.0367 Occurrence Handle1:CAS:528:DC%2BD3MXhslyit70%3D

    Article  CAS  Google Scholar 

  48. AA Odenyo PO Osuji (1998) ArticleTitleTannin-tolerant ruminal bacteria from East African ruminants Can J Microbiol 44 905–909 Occurrence Handle10.1139/cjm-44-9-905 Occurrence Handle9851029 Occurrence Handle1:CAS:528:DyaK1cXnvFyktrw%3D

    Article  PubMed  CAS  Google Scholar 

  49. AA Odenyo PO Osuji O Karanfil K Adinew (1997) ArticleTitleMicrobiological evaluation of Acacia angustissima as a protein supplement for sheep Anim Feed Sci Technol 65 99–112 Occurrence Handle10.1016/S0377-8401(96)01087-5

    Article  Google Scholar 

  50. R Osawa (1990) ArticleTitleFormation of a clear zone on tannin-treated brain heart infusion agar by a Streptococcus sp. isolated from feces of koalas Appl Environ Microbiol 56 829–831 Occurrence Handle2180375 Occurrence Handle1:STN:280:DyaK3c7pslajsg%3D%3D

    PubMed  CAS  Google Scholar 

  51. R Osawa K Kuroiso S Goto A Shimizu (2000) ArticleTitleIsolation of tannin-degrading Lactobacilli from humans and fermented foods Appl Environ Microbiol 66 3093–3097 Occurrence Handle10.1128/AEM.66.7.3093-3097.2000 Occurrence Handle10877812 Occurrence Handle1:CAS:528:DC%2BD3cXkslKltLs%3D

    Article  PubMed  CAS  Google Scholar 

  52. R Osawa F Rainey T Fujisawa E Lang HJ Busse TP Walsh E Stackebrandt (1995) ArticleTitleLonepinella koalarum gen. nov., sp. nov., a new tannin–protein complex degrading bacterium Syst Appl Microbiol 18 368–373 Occurrence Handle1:CAS:528:DyaK28XhsFWls7w%3D

    CAS  Google Scholar 

  53. RO Osawa (1992) ArticleTitleTannin–protein complex-degrading enterobacteria isolated from the alimentary tracts of koalas and a selective medium for their enumeration Appl Environ Microbiol 58 1754–1759 Occurrence Handle1622248 Occurrence Handle1:CAS:528:DyaK38XktVCjsrY%3D

    PubMed  CAS  Google Scholar 

  54. RO Osawa T Fujisowa LI Sly (1995) ArticleTitleStreptococcus gallolyticus sp. nov. gallate degrading organisms formerly assigned to Streptococcus bovis Syst Appl Microbiol 18 74–79

    Google Scholar 

  55. AN Pell TK Woolston KE Nelson P Schofield (2000) Tannins: biological activity and bacterial tolerance JD Brooker (Eds) Tannins in Livestock and Human Nutrition, Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 92 EditionNumber1 Australian Centre for International Agricultural Research Adelaide, Australia 121–126

    Google Scholar 

  56. RA Perez-Maldonado BW Norton (1996) ArticleTitleDigestion of 14C-labelled condensed tannins from Desmodium intortum in sheep and goats Br J Nutr 76 501–513 Occurrence Handle8942359 Occurrence Handle1:CAS:528:DyaK28Xnt1Cgurk%3D

    PubMed  CAS  Google Scholar 

  57. H Pinkart D White (1997) ArticleTitlePhosolipid biosynthesis and solvent tolerance in Pseudomonas putida strains J Bacteriol 179 4219–4226 Occurrence Handle9209036 Occurrence Handle1:CAS:528:DyaK2sXkt1Gls7w%3D

    PubMed  CAS  Google Scholar 

  58. JL Ramos E Duque JJ Rodriguez-Herva P Godoy A Haidour F Reyes A Fernandez-Barrero (1997) ArticleTitleMechanisms for solvent tolerance in bacteria J Biol Chem 272 3887–3890 Occurrence Handle9020089 Occurrence Handle1:CAS:528:DyaK2sXht1Olsb4%3D

    PubMed  CAS  Google Scholar 

  59. AK Ratty J Sunamoto NP Das (1988) ArticleTitleInteraction of flavonoids with 1,1-diphenyl-2-picrylhydrazyl free radical, liposomal membranes and soybean lipoxygenase-1 Biochem Pharmacol 37 989–995 Occurrence Handle10.1016/0006-2952(88)90499-6 Occurrence Handle3128297 Occurrence Handle1:CAS:528:DyaL1cXktVSit7w%3D

    Article  PubMed  CAS  Google Scholar 

  60. N Rozes C Peres (1998) ArticleTitleEffects of phenolic compounds on the growth and the fatty acid composition of Lactobacillus plantarum Appl Microbiol Biotechnol 49 108–111 Occurrence Handle1:CAS:528:DyaK1cXhtVanurs%3D

    CAS  Google Scholar 

  61. S Sakanaka M Aizawa M Kim T Yamamoto (1996) ArticleTitleInhibitory effects of green tea polyphenols on growth and cellular adherence of an oral bacterium, Porphyromonas gingivalis Biosci Biotechnol Biochem 60 745–749 Occurrence Handle8704303 Occurrence Handle1:CAS:528:DyaK28Xjtl2ru74%3D

    PubMed  CAS  Google Scholar 

  62. A Scalbert (1991) ArticleTitleAntimicrobial properties of tannins Phytochemistry 30 3875–3883 Occurrence Handle10.1016/0031-9422(91)83426-L Occurrence Handle1:CAS:528:DyaK38XnvF2ksg%3D%3D

    Article  CAS  Google Scholar 

  63. H Schneider M Blaut (2000) ArticleTitleAnaerobic degradation of flavonoids by Eubacterium ramulus Arch Microbiol 173 71–75 Occurrence Handle10.1007/s002030050010 Occurrence Handle10648107 Occurrence Handle1:CAS:528:DC%2BD3cXhslKlsbY%3D

    Article  PubMed  CAS  Google Scholar 

  64. P Schofield DM Mbugua AN Pell (2001) ArticleTitleAnalysis of condensed tannins: a review Anim Feed Sci Technol 91 21–40 Occurrence Handle10.1016/S0377-8401(01)00228-0 Occurrence Handle1:CAS:528:DC%2BD3MXjslSms74%3D

    Article  CAS  Google Scholar 

  65. JL Sebat AJ Paszczynski MS Cortese RL Crawford (2001) ArticleTitleAntimicrobial properties of pyridine-2,6-dithiocarboxylic acid, a metal chelator produced by Pseudomonas spp Appl Environ Microbiol 67 3934–3942 Occurrence Handle10.1128/AEM.67.9.3934-3942.2001 Occurrence Handle11525988 Occurrence Handle1:CAS:528:DC%2BD3MXmslWjurs%3D

    Article  PubMed  CAS  Google Scholar 

  66. N Silanikove N Gilboa Z Nitsan (2001) ArticleTitleEffect 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 Res 40 95–99 Occurrence Handle10.1016/S0921-4488(00)00209-1 Occurrence Handle11259880

    Article  PubMed  Google Scholar 

  67. LI Sly MM Cahill RO Osawa T Fujisawa (1997) ArticleTitleThe tannin-degrading species Streptococcus gallolyticus and Streptococcus caprinus are subjective synonyms Int J Syst Bacteriol 47 893–894 Occurrence Handle9226925 Occurrence Handle1:STN:280:DyaK2szntVKiuw%3D%3D

    PubMed  CAS  Google Scholar 

  68. AH Smith J Imlay RI Mackie (2003) ArticleTitleIncreasing the oxidative stress response allows Escherichia coli to overcome inhibitory effects of condensed tannins Appl Environ Microbiol 69 3406–3411 Occurrence Handle12788743 Occurrence Handle1:CAS:528:DC%2BD3sXks1Gltbo%3D

    PubMed  CAS  Google Scholar 

  69. AH Smith RI Mackie (2004) ArticleTitleThe effect of condensed tannins on bacterial diversity and metabolic activity in the rat gastrointestinal tract Appl Environ Microbiol 70 1104–1115 Occurrence Handle14766594 Occurrence Handle1:CAS:528:DC%2BD2cXhs1CgsL4%3D

    PubMed  CAS  Google Scholar 

  70. AH Smith AA Odenyo PO Osuji MA Wallig FE Kandil DS Seigler RI Mackie (2001) ArticleTitleEvaluation of toxicity of Acacia angustissima in a rat bioassay Anim Feed Sci Technol 91 41–57 Occurrence Handle10.1016/S0377-8401(01)00230-9 Occurrence Handle1:CAS:528:DC%2BD3MXjslSms7w%3D

    Article  CAS  Google Scholar 

  71. CM Spencer Y Cai R Martin SH Gaffney PN Goulding D Magnolato TH Lilley E Haslam (1988) ArticleTitlePolyphenol complexation—some thoughts and observations Phytochemistry 27 2397–2409 Occurrence Handle1:CAS:528:DyaL1cXlsVyjsbs%3D

    CAS  Google Scholar 

  72. G Sreerangaraju U Krishnamoorthy MM Kailas (2000) ArticleTitleEvaluation of Bengal gram (Cicer arietinum) husk a source of tannin and its interference in rumen and post-rumen nutrient digestion in sheep Anim Feed Sci Technol 85 131–138 Occurrence Handle10.1016/S0377-8401(00)00131-0 Occurrence Handle1:CAS:528:DC%2BD3cXjs1GksLc%3D

    Article  CAS  Google Scholar 

  73. J Terao M Piskula Q Yao (1994) ArticleTitleProtective effect of epicatechin, epicatechin gallate, and quercetin on lipid peroxidation in phospholipid bilayers Arch Biochem Biophys 308 278–284 Occurrence Handle10.1006/abbi.1994.1039 Occurrence Handle8311465 Occurrence Handle1:STN:280:DyaK2c7ksFSqsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  74. TH Terrill GC Waghorn DJ Woolley WC McNabb TN Barry (1994) ArticleTitleAssay and digestion of 14C-labelled condensed tannins in the gastrointestinal tract of sheep Br J Nutr 72 467–477 Occurrence Handle7947660 Occurrence Handle1:CAS:528:DyaK2cXmsFCmtbc%3D Occurrence Handle10.1079/BJN19940048

    Article  PubMed  CAS  Google Scholar 

  75. GR Tompkins NL O'Dell IT Bryson CB Pennington (2001) ArticleTitleThe effects of dietary ferric iron and iron deprivation on the bacterial composition of the mouse intestine Curr Microbiol 43 38–42 Occurrence Handle10.1007/s002840010257 Occurrence Handle11375662 Occurrence Handle1:CAS:528:DC%2BD3MXjslKgsL0%3D

    Article  PubMed  CAS  Google Scholar 

  76. H Tsuchiya (1999) ArticleTitleEffects of green tea catechins on membrane fluidity Pharmacology 59 34–44 Occurrence Handle10.1159/000028303 Occurrence Handle10352424 Occurrence Handle1:CAS:528:DyaK1MXktFelsbc%3D

    Article  PubMed  CAS  Google Scholar 

  77. J Winter LH Moore VR Dowell SuffixJr VD Bokkenheuser (1989) ArticleTitleC-ring cleavage of flavonoids by human intestinal bacteria Appl Environ Microbiol 55 1203–1208 Occurrence Handle2757380 Occurrence Handle1:CAS:528:DyaL1MXkt1Sltrc%3D

    PubMed  CAS  Google Scholar 

  78. KG Wiryawan B Tangendjaja A Suryahadi (2000) Tannin degrading bacteria from Indonesian ruminants JD Brooker (Eds) Tannins in Livestock and Human Nutrition: Proceedings of an International Workshop, Adelaide, Australia. ACIAR Proceedings No. 92 EditionNumber1 Australian Centre for International Agricultural Research Adelaide, Australia 123–126

    Google Scholar 

  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, LA

  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, Mexico

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Texas, Southwestern Medical Center, Dallas, TX, 75390, USA

    Alexandra H. Smith

  2. Laboratory of Microbiology, Wageningen University, 6703 CT, Wageningen, The Netherlands

    Erwin Zoetendal

  3. Department of Animal Sciences, University of Illinois, 1207 W. Gregory Dr, Urbana, IL, 61801, USA

    Roderick I. Mackie

  4. Division of Nutritional Sciences, University of Illinois, 1207 W. Gregory Dr., Urbana, IL, 61801, USA

    Roderick I. Mackie

Authors
  1. Alexandra H. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erwin Zoetendal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roderick I. Mackie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roderick I. Mackie.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, A.H., Zoetendal, E. & Mackie, R.I. Bacterial Mechanisms to Overcome Inhibitory Effects of Dietary Tannins. Microb Ecol 50, 197–205 (2005). https://doi.org/10.1007/s00248-004-0180-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-004-0180-x

Keywords

Search

Navigation