Applied Microbiology and Biotechnology

, Volume 64, Issue 4, pp 447–454 | Cite as

Properties and applications of microbial transglutaminase

  • K. Yokoyama
  • N. Nio
  • Y. Kikuchi


Some properties and applications of the transglutaminase (TGase) referred to as microbial TGase (MTGase), derived from a variant of Streptomyces mobaraensis (formerly classified as Streptoverticillium mobaraense), are described. MTGase cross-linked most food proteins, such as caseins, soybean globulins, gluten, actin, myosins, and egg proteins, as efficiently as mammalian TGases by forming an ε-(γ-glutamyl)lysine bond. However, unlike many other TGases, MTGase is calcium-independent and has a relatively low molecular weight. Both of these properties are of advantage in industrial applications; a number of studies have illustrated the potential of MTGase in food processing and other areas. The crystal structure of MTGase has been solved. It provides basic structural information on the MTGase and accounts well for its characteristics. Moreover, an efficient method for producing extracellular MTGase has been established using Corynebacterium glutamicum. MTGase may be expected to find many uses in both food and non-food applications.


Streptomyces Food Protein Corynebacterium Glutamicum Acyl Donor Acyl Acceptor 
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.


  1. Aeschlimann D, Paulsson M (1994) Transglutaminases: protein cross-linking enzymes in tissues and body fluids. Thromb Haemost 71:402–415PubMedGoogle Scholar
  2. Ando H, Adachi M, Umeda K, Matsuura A, Nonaka M, Uchio R, Tanaka H, Motoki M (1989) Purification and characteristics of a novel transglutaminase derived from microorganism. Agric Biol Chem 53:2613–2617Google Scholar
  3. Bishop PD, Teller DC, Smith RA, Lasser GW, Gilbert T, Seale RL (1990) Expression, purification, and characterization of human factor XIII in Saccharomyces cerevisiae. Biochemistry 29:1861–1869PubMedGoogle Scholar
  4. Chung SI, Lewis MS, Folk JE (1974) Relationships of the catalytic properties of human plasma and platelet transglutaminases (activated blood coagulation factor XIII) to their subunit structures. J Biol Chem 249:940–950PubMedGoogle Scholar
  5. Date M, Yokoyama K, Umezawa Y, Matsui H, Kikuchi Y (2003) Production of native-type Streptoverticillium mobaraense transglutaminase in Corynebacterium glutamicum. Appl Environ Microbiol 69:3011–3014CrossRefPubMedGoogle Scholar
  6. Enzyme Nomenclature (1992) Nomenclature Committee of the International Union of Biochemistry and Molecular Biology (eds) Academic Press, San Diego, Calif.Google Scholar
  7. Fink ML, Chung SI, Folk JE (1980) γ-Glutamine cyclotransferase: specificity toward ε-(γ-glutamyl)-l-lysine and related compounds. Proc Natl Acad Sci USA 77:4564–4568PubMedGoogle Scholar
  8. Finot PA, Mottu F, Bujard E, Mauron J (1978) In: Friedman M (ed) Nutritional improvement of food and foods proteins. Plenum Press, London, pp 549–570Google Scholar
  9. Friedman M, Finot PA (1990) Nutritional improvement of bread with lysine and γ-glutamyllysine. J Agric Food Chem 38:2011–2020Google Scholar
  10. Hornyak TJ, Bishop PD, Shafer JA (1989) α-Thrombin-catalyzed activation of human platelet factor XIII: relationship between proteolysis and factor XIIIa activity. Biochemistry 28:7326–7332PubMedGoogle Scholar
  11. Ikeda M, Nakagawa S (2003) The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl Microbiol Biotechnol 62:99–109CrossRefPubMedGoogle Scholar
  12. Ikura K, Sasaki R, Motoki M (1992) Use of transglutaminase in quality-improvement and processing of food proteins. Comments Agric Food Chem 2:389–407Google Scholar
  13. Ikura K, Nasu T, Yokota H, Tsuchiya Y, Sasaki R, Chiba H (1998) Amino acid sequence of guinea pig liver transglutaminase. Biochemistry 27:2898–2905Google Scholar
  14. Iwami K, Yasumoto K (1986) Amine-binding capacities of food proteins in transglutaminase reaction and digestibility of wheat gliadin with ε-attached lysine. J Sci Food Agric 37:495–503Google Scholar
  15. Kanaji T, Ozaki H, Takao T, Kawajiri H, Ide H, Motoki M, Shimonishi Y (1993) Primary structure of microbial transglutaminase from Streptoverticillium sp. strain s-8112. J Biol Chem 268:11565–11572PubMedGoogle Scholar
  16. Kang IJ, Matsumura Y, Ikura K, Motoki M, Sakamoto H, Mori T (1994) Gelation and properties of soybean glycinin in a transglutaminase-catalyzed system. J Agric Food Chem 42:159–165Google Scholar
  17. Kashiwagi T, Yokoyama K, Ishikawa K, Ono K, Ejima D, Matui H, Suzuki E (2002) Crystal structure of microbial transglutaminase from Streptoverticillium mobaraense. J Biol Chem 277 46:44252–44260CrossRefGoogle Scholar
  18. Kato A, Wada T, Kobayashi K, Seguro K, Motoki M (1991) Ovomucin-food protein conjugates prepared through the transglutaminase reaction. Agric Biol Chem 55:1027–1031Google Scholar
  19. Kikuchi Y, Date M, Umezawa Y, Yokoyama K, Heima H, Matsui H (2002) Method for the secretion and production protein. International Patent Cooperation Treaty patent WO02/081694Google Scholar
  20. Kikuchi Y, Date M, Yokoyama K, Umezawa Y, Matsui H (2003) Secretion of active-form Streptoverticillium mobaraense transglutaminase by Corynebacterium glutamicum: processing of the pro-domain by a co-secreted subtilisin-like protease from Streptomyces albogriseolus. Appl Environ Microbiol 69:358–366CrossRefPubMedGoogle Scholar
  21. Krämer R (1994) Secretion of amino acids by bacteria: physiology and mechanism. FEMS Microbiol Rev 12:75–94CrossRefGoogle Scholar
  22. Kumazawa Y, Sakamoto H, Kawajiri H, Seguro K, Motoki M (1996a) Determination of ε-(γ-glutamyl)lysine in several fish eggs and muscle proteins. Fish Sci 62:331–332Google Scholar
  23. Kumazawa Y, Nakanishi K, Yasueda H, Motoki M (1996b) Purification and characterization of transglutaminase from walleye pollack liver. Fish Sci 62:959–964Google Scholar
  24. Kuraishi C, Sakamoto J, Soeda T (1996) The usefulness of transglutaminase for food processing. biotechnology for improved foods and flavors. In: Takeoka GR, Teranishi R, Williams PJ, Kobayashi A (eds) Biotechnology for improved foods and flavors. ACS symposium series 637 pp 29–38Google Scholar
  25. Kurth L, Rogers PJ (1984) Transglutaminase catalyzed crosslinking of myosin to soya protein, casein, and gluten. J Food Sci 49:573–576Google Scholar
  26. Liebl W (1991) The genus Corynebacterium—nonmedical. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, New York Berlin Heidelberg, pp 1157–1171Google Scholar
  27. Malumbres M, Gil JA, Martin JF (1993) Codon preference in Corynebacteria. Gene 134:15–24CrossRefPubMedGoogle Scholar
  28. Meister A, Tate SS, Griffith OW (1981) γ-Glutamyl transpeptidase. Methods Enzymol 77:237–253PubMedGoogle Scholar
  29. Motoki M, Nio N (1983) Crosslinking between different food proteins by transglutaminase. J Food Sci 48:561–566Google Scholar
  30. Motoki M, Nio N, Takinami K (1984) Functional properties of food proteins polymerized by transglutaminase. Agric Biol Chem 48:1257–1261Google Scholar
  31. Motoki M, Seguro K, Nio N, Takinami K (1986) Glutamine-specific deamidation of transglutaminase. Agric Biol Chem 50:3025–3030Google Scholar
  32. Motoki M, Aso H, Seguro K, Nio N (1987a) αS1-Casein film prepared using transglutaminase. Agric Biol Chem 51:993–996Google Scholar
  33. Motoki M, Nio N, Takinami K (1987b) Functional properties of heterologous polymer prepared by transglutaminase. Agric Biol Chem 51:237–238Google Scholar
  34. Neilsen PM (1995) Reactions and potential industrial applications of transglutaminase. Review of literature and patents. Food Biotechol 9:119–156Google Scholar
  35. Nio N, Motoki M (1986) Gelation of protein emulsion by transglutaminase. Agric Biol Chem 50:1409–1412Google Scholar
  36. Nio N, Motoki M, Takinami K (1985) Gelation of casein and soybean globulins by transglutaminase. Agric Biol Chem 49:851–855Google Scholar
  37. Nio N, Motoki M, Takinami K (1986) Gelation mechanism of protein solutions by transglutaminase. Agric Biol Chem 48:851–855Google Scholar
  38. Noguchi K, Ishikawa K, Yokoyama K, Ohtsuka T, Nio N, Suzuki E (2001) Crystal structure of red sea bream transglutaminase. J Biol Chem 276 15:12055–12059CrossRefGoogle Scholar
  39. Nonaka M, Tanaka H, Okiyama A, Motoki M, Ando H, Umeda K, Matsuura A (1989) Polymerization of several proteins by Ca2+-independent transglutaminase derived from microorganisms. Agric Biol Chem 53:2619–2623Google Scholar
  40. Nonaka M, Sakamoto H, Toiguchi S, Kawajiri H, Soeda T, Motoki M (1992) Sodium caseinate and skim milk gels formed by incubation with microbial transglutaminase. J Food Sci 57:1214–1218Google Scholar
  41. Nonaka M, Matsuura Y, Nakano K, Motoki M (1997) Improvement of the pH-solubility profile of sodium caseinate by using Ca2+-independent microbial transglutaminase with gelatin. Food Hydrocolloids 11:347–349Google Scholar
  42. Pasternack R, Dorsch S, Otterbach JT, Robenek IR, Wolf S, Fuchsbauer HL (1998) Bacterial pro-transglutaminase from Streptoverticillium mobaraense: purification, characterization and sequence of zymogen. Eur J Biochem 257:570–576CrossRefPubMedGoogle Scholar
  43. Sakamoto H, Kumazawa Y, Kawajiri H, Motoki M (1995) ε-(γ-Glutamyl)lysine crosslink distribution in foods as determined by improved method. J Food Sci 60:416–419Google Scholar
  44. Sakamoto H, Yamazaki K, Kaga C, Yamamoto Y, Ito R, Kurosawa Y (1996) Strength enhancement by addition of microbial transglutaminase during Chinese noodle processing. Nippon Shokuhin Kagaku Kaishi 43:598–602Google Scholar
  45. Seguro K, Kumazawa Y, Kuraishi C, Sakamoto H, Motoki M (1994) Trends Jpn Soy Protein Res Inform 5:308–313Google Scholar
  46. Seguro K, Kumazawa Y, Ohtsuka T, Toiguchi S, Motoki M (1995a) Microbial transglutaminase and ε-(γ-glutamyl)lysine crosslink effects on elastic properties of kamaboko gel. J Food Sci 60:305–311Google Scholar
  47. Seguro K, Kumazawa Y, Ohtsuka T, Ide H, Nio N, Motoki M, Kubota K (1995b) ε-(γ-Glutamyl)lysine: hydrolysis by γ-glutamyl transferase of different origins, when free or protein bound. J Agric Food Chem 43:1977–1981Google Scholar
  48. Seki N, Uno H, Lee NH, Kimura I, Toyoda K, Fujita T, Arai K (1990) Transglutaminase activity in Alaska pollack muscle and surimi, and its reaction with myosin b. Nippon Suisan Gakkaishi 56:125–132Google Scholar
  49. Shimba N, Yokoyama K, Suzuki E (2002) NMR-based screening method for transglutaminase: rapid analysis of their substrate specificities and reaction rates. J Agric Food Chem 50:1330–1334Google Scholar
  50. Suzuki M, Taguchi S, Yamada S, Kojima S, Miura K, Momose H (1997) A novel member of the subtilisin-like protease family from Streptomyces albogriseolus. J Bacteriol 179:430–438PubMedGoogle Scholar
  51. Takehana S, Washizu K, Ando K, Koikeda S, Takeuchi K, Matsui H, Motoki M, Takagi H (1994) Chemical synthesis of the gene for microbial transglutaminase from Streptoverticillium and its expression in Escherichia coli. Biosci Biotechnol Biochem 58:88–92PubMedGoogle Scholar
  52. Washizu K, Ando K, Koikeda S, Hirose S, Matsuura A, Akagi H, Motoki M, Takeuchi K (1994) Molecular cloning of the gene for microbial transglutaminase from Streptoverticillium and its expression in Streptomyces lividans. Biosci Biotechnol Biochem 58:82–87PubMedGoogle Scholar
  53. Whitaker JR (1977) In: Feeney RE, Whitaker JR (eds) Food proteins-improvement through chemical and enzymatic modification. American Chemical Society, Washington, D.C., pp 95–105Google Scholar
  54. Wilson SA (1992) Modifying meat proteins via enzymatic crosslinking, proceedings of the 27th meat industry research conference, Hamilton, Meal Industry Research Institutes of New Zealand, Mirinz, pp 247–277Google Scholar
  55. Yasueda H, Nakanishi K, Kumazawa Y, Nagase K, Motoki M, Matsui H (1995) Tissue-type transglutaminase from red sea bream (Pagrus major) sequence analysis of the cDNA and functional expression in Escherichia coli. Eur J Biol 232:411–419Google Scholar
  56. Yee VC, Pedersen LC, Trong IL, Bishop PD, Stenkamp RE, Teller DC (1994) Tree-dimensional structure of a transglutaminase: human blood coagulation factor XIII. Proc Natl Acad Sci USA 91:7296–7300PubMedGoogle Scholar
  57. Yokoyama K, Nakamura N, Saguaro K, Kubota K (2000) Overproduction of microbial transglutaminase in Escherichia coli, in vitro refolding, and characterization of the refolded form. Biosci Biotechnol Biochem 64:1263–1270PubMedGoogle Scholar
  58. Zhu Y, Rinzema A, Tramper J, Bol J (1995) Microbial transglutaminase—a review of its production and application in food processing. Appl Microbiol Biotechnol 44:277–282CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Ajinomoto Institute of Life SciencesKawasaki Japan

Personalised recommendations