Skip to main content
SpringerLink
Log in

Characterization of a bacterial tannase from Streptococcus gallolyticus UCN34 suitable for tannin biodegradation

  • Biotechnologically relevant enzymes and proteins
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The gene in the locus GALLO_1609 from Streptococcus gallolyticus UCN34 was cloned and expressed as an active protein in Escherichia coli BL21 (DE3). The protein was named TanSg1 since it shows similarity to bacterial tannases previously described. The recombinant strain produced His-tagged TanSg1 which was purified by affinity chromatography. Purified TanSg1 protein showed tannase activity, having a specific activity of 577 U/mg which is 41 % higher than the activity of Lactobacillus plantarum tannase. Remarkably, TanSg1 displayed optimum catalytic activity at pH 6–8 and 50–70 °C and showed high stability over a broad range of temperatures. It retained 25 % of its relative activity after prolonged incubation at 45 °C. The specific activity of TanSg1 is enhanced by the divalent cation Ca2+ and is dramatically reduced by Zn2+ and Hg2+. The enzyme was highly specific for gallate and protocatechuate esters and showed no catalytic activity against other phenolic esters. The protein TanSg1 hydrolyzes efficiently tannic acid, a complex and polymeric gallotanin, allowing its complete conversion to gallic acid, a potent antioxidant. From its biochemical properties, TanSg1 is a tannase with potential industrial interest regarding the biodegradation of tannin waste or its bioconversion into biologically active products.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aguilar CN, Gutiérrez-Sánchez G (2001) Review: sources, properties, applications and potential uses of tannin acyl hydrolase. Food Sci Tech Int 7:373–382

    Article  CAS  Google Scholar 

  • Aguilar CN, Rodríguez R, Gutiérrez-Sánchez G, Augur C, Favela-Torres E, Prado-Barragan LA, Ramirez-Coronel A, Contreras-Esquivel JC (2007) Microbial tannases: advances and perspectives. Appl Microbiol Biotechnol 76:47–59

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Jana A, Pati BR, Mondal KC, Das Mohapatra PK (2012) Characterization of tannase protein sequences of bacteria and fungi: an in silico study. Protein J 31:306–327

    Article  CAS  PubMed  Google Scholar 

  • Belmares R, Contreras-Esquivel JC, Rodríguez-Herrera R, Ramirez Coronel A, Aguilar CN (2004) Microbial production of tannase: an enzyme with potential use in food industry. Lebensm-Wiss u-Technol 37:857–864

    Article  CAS  Google Scholar 

  • Cantos E, Espin JC, López-Bote C, de la Hoz L, Ordoñez JA, Tomás-Barberán FA (2003) Phenolic compounds and fatty acids from acorns (Quercus spp.), the main constituent of free-ranged Iberian pigs. J Agric Food Chem 51:6248–6255

    Article  CAS  PubMed  Google Scholar 

  • Chamkha M, Patel BKC, Traore A, Garcia J-L, Labat M (2002) Isolation from a shea cake digester of a tannin-degrading Streptococcus gallolyticus strain that decarboxylates protocatechuic acid hydroxycinnamic acids, and emendation of the species. Int J Systm Evol Microbiol 52:939–944

    Article  CAS  Google Scholar 

  • Chávez-González M, Rodríguez-Durán LV, Balagurusamy N, Prado-Barragán A, Rodríguez R, Contreras JC, Aguilar CN (2012) Biotechnological advances and challenges of tannase: an overview. Food Bioproc Technol 5:445–459

    Article  Google Scholar 

  • Curiel JA, Rodríguez H, Acebrón I, Mancheño JM, de las Rivas B, Muñoz R (2009) Production and physicochemical properties of recombinant Lactobacillus plantarum tannase. J Agric Food Chem 57:6224–6230

    Article  CAS  PubMed  Google Scholar 

  • Curiel JA, de las Rivas B, Mancheño JM, Muñoz R (2011) The pURI family of expression vectors: a versatile set of ligation independent cloning plasmids for producing recombinant His-fusion proteins. Prot Expr Purif 76:44–53

    Article  CAS  Google Scholar 

  • Hakkinen SH, Torronen AR (2000) Content of flavonols and selected phenolic acids in strawberries and Vaccinium species: influence of cultivar, cultivation site and technique. Food Res Int 33:517–524

    Article  CAS  Google Scholar 

  • Inoue KH, Hagerman AE (1988) Determination of gallotannins with rhodanine. Anal Biochem 169:363–369

    Article  CAS  PubMed  Google Scholar 

  • Iwamoto K, Tsuruta H, Nishitaini Y, Osawa R (2008) Identification and cloning of a gene encoding tannase (tannin acylhydrolase) from Lactobacillus plantarum ATCC 14917T. Syst Appl Microbiol 31:269–277

    Article  CAS  PubMed  Google Scholar 

  • Lekha PK, Lonsane BK (1997) Production and application of tannin acyl hydrolase: state of the art. Adv Appl Microb 44:212–260

    Google Scholar 

  • Mingshu L, Kai Y, Quiang H, Dongying J (2006) Biodegradation of gallotannins and ellagitannins. J Basic Microbiol 46:68–84

    Article  Google Scholar 

  • Mueller-Harvey I (2001) Analysis of hydrolysable tannins. Anim Feed Sci Technol 91:3–20

    Article  CAS  Google Scholar 

  • Noguchi N, Ohashi T, Shiratori T, Narui K, Hagiwara T, Ko M, Watanabe K, Miyahara T, Taira S, Moriyasu F, Sasatsu M (2007) Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene. J Gastroenterol 42:346–351

    Article  CAS  PubMed  Google Scholar 

  • Ordoudi SA, Tsimidou MZ (2006) Crocin bleaching assay (CBA) in structure-radical scavenging activity studies of selected phenolic compounds. J Agric Food Chem 54:9347–9356

    Article  CAS  PubMed  Google Scholar 

  • Osawa R, Walsh TP (1993) A visual reading method for detection of bacterial tannase. Appl Environ Microbiol 59:1251–1252

    CAS  PubMed Central  PubMed  Google Scholar 

  • Osawa R, Fujisawa T, Sly LI (1995) Streptococcus gallolyticus sp. nov.; gallate degrading organisms formerly assigned to Streptococcus bovis. Syst Appl Microbiol 18:74–78

    Article  Google Scholar 

  • Ren B, Wu M, Wang Q, Peng X, Wen H, McKinstry WJ, Chen Q (2013) Crystal structure of tannase from Lactobacillus plantarum. J Mol Biol 425:2737–2751

    Article  CAS  PubMed  Google Scholar 

  • Rusniok C, Couvé E, da Cunha V, El Gana R, Zidane N, Bouchier C, Poyart C, Leclercq R, Trieu-Cuot P, Glaser P (2010) Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J Bacteriol 192:2266–2276

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sharma KP, John PJ (2011) Purification and characterization of tannase and tannase gene from Enterobacter sp. Process Biochem 46:240–244

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Serrano J, Puupponen-Pimiä R, Dauer A, Aura A-M, Saura-Calixto F (2009) Tannins: current knowledge of food sources, intake, bioavailability and biological effects. Mol Nutr Food Res 53:310–S329

    Article  Google Scholar 

  • Sly LI, Cahill M, Osawa R, Fujisawa T (1997) The tannin-degrading species Streptococcus gallolyticus and Streptococcus caprinus are subjective synonyms. Int J Syst Bacteriol 47:893–894

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by grants AGL2011-22745, S2009/AGR-1469 (ALIBIRD) (Comunidad de Madrid), and RM2012-00004 (INIA). We are grateful to M. V. Santamaría for her technical assistance. N. Jiménez is a recipient of a FPI fellowship from the MINECO.

Author information

Authors and Affiliations

  1. Laboratorio de Biotecnología Bacteriana, Instituto de Ciencia y Tecnología de Alimentos y Nutrición, ICTAN-CSIC, Juan de la Cierva 3, 28006, Madrid, Spain

    Natalia Jiménez, José María Barcenilla, Félix López de Felipe, Blanca de las Rivas & Rosario Muñoz

Authors
  1. Natalia Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José María Barcenilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Félix López de Felipe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Blanca de las Rivas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rosario Muñoz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosario Muñoz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiménez, N., Barcenilla, J.M., de Felipe, F.L. et al. Characterization of a bacterial tannase from Streptococcus gallolyticus UCN34 suitable for tannin biodegradation. Appl Microbiol Biotechnol 98, 6329–6337 (2014). https://doi.org/10.1007/s00253-014-5603-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-5603-0

Keywords

Search

Navigation