1887

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Volume 145, Issue 12

Family 19 chitinases of species: characterization and distribution

The GenBank accession numbers for the sequences determined in this work are AB031745–AB031757 inclusive.

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Abstract

Chitinase C from HUT6037, described in 1997, is the first family 19 chitinase found in an organism other than higher plants. In this study, some properties of chitinase C were compared with those of family 18 bacterial chitinases, and the distribution of family 19 chitinases in species was investigated. The specific hydrolysing activity of chitinase C against soluble and insoluble chitinous substrates was markedly higher than those of bacterial family 18 chitinases. Chitinase C exhibited marked antifungal activity, whereas the other bacterial chitinases examined had no antifungal activity. Chitinase C was insensitive to allosamidin, whereas the family 18 bacterial chitinases were sensitive. Taking advantage of this insensitivity to allosamidin, a search was made for family 19 chitinases in various species. Chitinases insensitive to allosamidin were detected in the culture supernatants of all tested species. Southern hybridization analysis using a labelled DNA fragment corresponding to the catalytic domain of chitinase C strongly suggested that these species have genes similar to the gene of HUT6037. DNA fragments corresponding to the major part of the catalytic domains were amplified by PCR. The amplified fragments encoded amino acid sequences very similar to that of the corresponding region of chitinase C. Therefore, it was concluded that species generally possess family 19 chitinases which are very similar to chitinase C. Comparison of their amino acid sequences with those of plant family 19 chitinases revealed that family 19 chitinases are class IV type in terms of the presence and positions of deletions of amino acid sequences which are characteristic of plant class IV chitinases.

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Keyword(s): allosamidin , chitinase and Streptomyces
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1999-12-01
2024-04-18
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References

  1. Alam M. M., Nikaidou N., Tanaka H., Watanabe T. 1995; Cloning and sequencing of chiC gene of Bacillus circulans WL-12 and relationship of its product to some other chitinases and chitinase-like proteins. . J Ferment Bioeng 80:454–461 [CrossRef]
     [Google Scholar]
  2. Ames G. F. L. 1974; Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs. J Biol Chem 249:634–644
     [Google Scholar]
  3. Armand S., Tomita H., Heyraud A., Gey C., Watanabe T., Henrissat B. 1994; Stereochemical course of hydrolysis reaction catalyzed by chitinase A1 and D from Bacillus circulans WL-12. FEBS Lett 343:177–180 [CrossRef]
     [Google Scholar]
  4. Brameld K. A., Shrader D. W. D., Imperiali B., Goddard W. A. III 1998; Substrate assistance in the mechanism of family 18 chitinases: theoretical studies of potential intermediates and inhibitor. J Mol Biol 280:913–923 [CrossRef]
     [Google Scholar]
  5. Broekaert W. F., Parijs J. V., Allen A. K., Peumans W. J. 1988; Comparison of some molecular, enzymatic and antifungal properties of chitinases from thorn- apple, tobacco and wheat. Physiol Mol Plant Pathol 33:319–331 [CrossRef]
     [Google Scholar]
  6. Collinge D. B., Kragh K. M., Mikkelsen J. D., Nielsen K. K., Rasmussen U., Vad K. 1993; Plant chitinases. Plant J 3:31–40 [CrossRef]
     [Google Scholar]
  7. Davies G., Henrissat B. 1995; Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859 [CrossRef]
     [Google Scholar]
  8. Fukamizo T., Koga D., Goto S. 1995; Comparative biochemistry of chitinase – anomeric form of reaction products. . Biosci Biotechnol Biochem 59:311–313 [CrossRef]
     [Google Scholar]
  9. Garcia-Casado G., Collada C., Allona I., Casado R., Pacios L. F., Aragoncillo C., Gomez L. 1998; Site-directed mutagenesis of active site residues in a class I endochitinase from chestnut seeds. . Glycobiology 8:1021–1028 [CrossRef]
     [Google Scholar]
  10. Hamel F., Boivin R., Tremblay C., Bellemare G. 1997; Structural and evolutionary relationships among chitinases of flowering plants. J Mol Evol 44:614–624 [CrossRef]
     [Google Scholar]
  11. Hart P. J., Pfluger, H. D., Monzingo, A. F., Hollis T., Robertus J. D. 1995; The refined crystal structure of an endochitinase from Hordeum vulgare L. seeds at 1·8 Å resolution. . J Mol Biol 248:402–413
     [Google Scholar]
  12. Henrissat B. 1991; A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316
     [Google Scholar]
  13. Henrissat B., Bairoch A. 1993; New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 293:781–788
     [Google Scholar]
  14. Hopwood D. A., Bibb M. J., Chater K. F., Kieser T., Bruton C. J., Kieser H. M., Lydiate D. L., Smith C. P., Ward J. M., Schrempf H. S. 1985 Genetic Manipulation of Streptomyces: a Laboratory Manual Norwich, UK: John Innes Foundation;
     [Google Scholar]
  15. Imoto T., Yagishita K. 1971; A simple activity measurement of lysozyme. Agric Biol Chem 35:1154–1156 [CrossRef]
     [Google Scholar]
  16. Iseli B., Boller T., Neuhaus J.-M. 1993; The N-terminal cysteine-rich domain of tobacco class I chitinase is essential for chitin binding but not for catalytic or antifungal activity. Plant Physiol 103:221–226 [CrossRef]
     [Google Scholar]
  17. Iseli B., Armand S., Boller T., Neuhaus J.-M., Henrissat B. 1996; Plant chitinases use two different hydrolytic mechanisms. FEBS Lett 382:186–188 [CrossRef]
     [Google Scholar]
  18. Jeuniaux C. 1966; Chitinase. Methods Enzymol 8:644–650
     [Google Scholar]
  19. Koga D., Isogai A., Sakuda S., Matsumoto S., Suzuki A., Kimura S. 1987; Specific inhibition of Bombyx mori chitinase by allosamidin. Agric Biol Chem 51:471–476 [CrossRef]
     [Google Scholar]
  20. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
     [Google Scholar]
  21. Leah R., Tommerup H., Svendsen I., Mundy J. 1991; Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J Biol Chem 266:1564–1573
     [Google Scholar]
  22. Manoil C., Beckwith J. 1986; A genetic approach to analyzing membrane protein topology. Science 233:1403–1408 [CrossRef]
     [Google Scholar]
  23. Mitsutomi M., Hata T., Kuwahara T. 1995; Purification and characterization of novel chitinases from Streptomyces griseus HUT6037. J Ferment Bioeng 80:153–158 [CrossRef]
     [Google Scholar]
  24. Mitsutomi M., Ueda M., Arai M., Ando A., Watanabe T. 1996; Action patterns of microbial chitinases and chitosanases on partially N-acetylated chitosan. Chitin Enzymol 2:273–284
     [Google Scholar]
  25. Mitsutomi M., Uchiyama A., Yamagami T., Watanabe T. 1997; Mode of action of family 19 chitinases. In Advances in Chitin Science pp. 250–255Edited by Domard A., Roberts G. A. F., Varum K. M. Lyon: Jacques André Publisher;
     [Google Scholar]
  26. Molano J., Duran A., Cabib E. 1977; A rapid and sensitive assay for chitinase using tritiated chitin. Anal Biochem 83:648–656 [CrossRef]
     [Google Scholar]
  27. Monreal J., Reese E. T. 1969; The chitinase of Serratia marcescens. Can J Microbiol 15:689–696 [CrossRef]
     [Google Scholar]
  28. Monzingo A. F., Marcotte E. M., Hart P. J., Robertus J. D. 1996; Chitinases, chitosanases, and lysozymes can be divided into prokaryotic and eukaryotic families sharing a conserved core. Nature Struct Biol 3:133–140 [CrossRef]
     [Google Scholar]
  29. Ohno T., Armand S., Hata T., Nikaidou N., Henrissat B., Mitsutomi M., Watanabe T. 1996; A modular family 19 chitinase found in the prokaryotic organism Streptomyces griseus HUT 6037. J Bacteriol 178:5065–5070
     [Google Scholar]
  30. Palomar J., Guasch J. F., Regue M., Vinas M. 1990; The effect of nuclease on transformation efficiency in Serratia marcescens. . FEMS Microbiol Lett 57:255–258
     [Google Scholar]
  31. Perrakis A., Tews I., Dauter Z., Oppenheim A. B., Chet I., Wilson K. S., Vorgias C. E. 1994; Crystal structure of a bacterial chitinase at 2·3 Å resolution. Structure 2:1169–1180 [CrossRef]
     [Google Scholar]
  32. Raikhel N. V., Lee H.-I., Broekaert W. F. 1993; Structure and function of chitin binding proteins. Annu Rev Plant Physiol Plant Mol Biol 44:591–615 [CrossRef]
     [Google Scholar]
  33. Roberts W. K., Selitrennikoff C. P. 1988; Plant and bacterial chitinases differ in antifungal activity. J Gen Microbiol 134:169–176
     [Google Scholar]
  34. Saito A., Fujii T., Yoneyama T., Redenbach M., Ohno T., Watanabe T., Miyashita K. 1999; High- multiplicity of chitinase genes in Streptomyces coelicolor A3(2). Biosci Biotechnol Biochem 63:710–718 [CrossRef]
     [Google Scholar]
  35. Sakuda S., Isogai A., Matsumoto S., Suzuki A. 1986; The structure of allosamidin, a novel insect chitinase inhibitor, produced by Streptomyces sp. . Tetrahedron Lett 27:2475–2478 [CrossRef]
     [Google Scholar]
  36. Schlumbaum A., Mauch F., Vögeli U., Boller T. 1986; Plant chitinases are potent inhibitors of fungal growth. Nature 324:365–367 [CrossRef]
     [Google Scholar]
  37. Shinshi H., Neuhaus, J.-M., Ryals J., Meins F. 1990; Structure of a tobacco endochitinase gene: evidence that different genes can arise by transposition of sequences encoding a cysteine-rich domain. Plant Mol Biol 14:357–368 [CrossRef]
     [Google Scholar]
  38. Shirling E. B., Gottlieb D. 1972; Cooperative description of type culture of Streptomyces. V. Additional descriptions. . Int J Syst Bacteriol 22:265–394 [CrossRef]
     [Google Scholar]
  39. Suzuki K., Suzuki M., Taiyoji M., Nikaidou N., Watanabe T. 1998; Chitin binding protein (CBP21) in the culture supernatant of Serratia marcescens 2170. . Biosci Biotechnol Biochem 62:128–135 [CrossRef]
     [Google Scholar]
  40. Suzuki K., Taiyoji M., Sugawara N., Nikaidou N., Henrissat B., Watanabe T. 1999; The third chitinase gene ( chiC) of Serratia marcescens 2170 and the relationship of its product to other bacterial chitinases. Biochem J 343:587–596 [CrossRef]
     [Google Scholar]
  41. Tanaka H., Phaff H. J. 1965; Enzymatic hydrolysis of yeast cell walls. I. Isolation of wall-decomposing organism and separation and purification of lytic enzymes. J Bacteriol 89:1570–1580
     [Google Scholar]
  42. Tashiro N., Miyahita K., Suzuki T. 1990; Taxonomic studies on the Streptomyces species, isolated as causal organisms of potato scab. . Ann Phytopathol Soc Jpn 56:73–82 [CrossRef]
     [Google Scholar]
  43. Terwisscha van Scheltinga, A. C., Kalk K. H., Beintema J. J., Dijkstra B. W. 1994; Crystal structure of hevamine, a plant defense protein with chitinase and lysozyme activity, and its complex with an inhibitor. Structure 2:1181–1189 [CrossRef]
     [Google Scholar]
  44. Tews I., Terwissha van Schentiga, A. C., Perrakis A., Wilson K. S., Dijkstra B. W. 1997; Substrate-assisted catalysis unifies two families of chitinolytic enzymes. . J Am Chem Soc 119:7954–7959 [CrossRef]
     [Google Scholar]
  45. Ueno H., Miyashita K., Sawada Y., Oba Y. 1990; Purification and some properties of extracellular chitinases from Streptomyces sp. S-84. . J Gen Appl Microbiol 36:377–392 [CrossRef]
     [Google Scholar]
  46. Watanabe T., Oyanagi W., Suzuki K., Tanaka H. 1990; Chitinase system of Bacillus circulans WL-12 and importance of chitinase A1 in chitin degradation. J Bacteriol 172:4017–4022
     [Google Scholar]
  47. Watanabe T., Kimura K., Sumiya T., Nikaidou N., Suzuki K., Suzuki M., Taiyoji M., Ferrer S., Regue M. 1997; Genetic analysis of the chitinase system of Serratia marcescens 2170. J Bacteriol 179:7111–7117
     [Google Scholar]
  48. Yamada H., Imoto T. 1981; A convenient synthesis of glycol chitin, a substrate of lysozyme. Carbohydr Res 92:160–162 [CrossRef]
     [Google Scholar]
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Family 19 chitinases of Streptomyces species: characterization and distributionThe GenBank accession numbers for the sequences determined in this work are AB031745–AB031757 inclusive.
Microbiology 145, 3353 (1999); https://doi.org/10.1099/00221287-145-12-3353
/content/journal/micro/10.1099/00221287-145-12-3353
/content/journal/micro/10.1099/00221287-145-12-3353
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