BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Identification of an Antifungal Chitinase from a Potential Biocontrol Agent, Bacillus cereus 28-9

  • Huang, Chien-Jui (Department of Plant Pathology and Microbiology, National Taiwan University) ;
  • Wang, Tang-Kai (Department of Plant Pathology and Microbiology, National Taiwan University) ;
  • Chung, Shu-Chun (Department of Plant Pathology and Microbiology, National Taiwan University) ;
  • Chen, Chao-Ying (Department of Plant Pathology and Microbiology, National Taiwan University)
  • Published : 2005.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Bacillus cereus 28-9 is a chitinolytic bacterium isolated from lily plant in Taiwan. This bacterium exhibited biocontrol potential on Botrytis leaf blight of lily as demonstrated by a detached leaf assay and dual culture assay. At least two chitinases (ChiCW and ChiCH) were excreted by B. cereus 28-9. The ChiCW-encoding gene was cloned and moderately expressed in Escherichia coli DH5$\alpha$. Near homogenous ChiCW was obtained from the periplasmic fraction of E. coli cells harboring chiCW by a purification procedure. An in vitro assay showed that the purified ChiCW had inhibitory activity on conidial germination of Botrytis elliptica, a major fungal pathogen of lily leaf blight.

Keywords

References

  1. Barboza-Corona, J. E., Nieto-Mazzocco, E., Velázquez-Robledo, R., Salcedo-Hernandez, R., Bautista, M., Jimenez, B. and Ibarra, J. E. (2003) Cloning, sequencing, and expression of the chitinase gene chiA74 from Bacillus thuringiensis. Appl. Environ. Microbiol. 69, 1023-1029 https://doi.org/10.1128/AEM.69.2.1023-1029.2003
  2. Bartnicki-Garcia, S. (1969) Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu. Rev. Microbiol. 22, 87-108 https://doi.org/10.1146/annurev.mi.22.100168.000511
  3. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 https://doi.org/10.1016/0003-2697(76)90527-3
  4. Brunel, B., Perissol, C., Fernandez, M., Boeufgras, J. M. and Le Petit, J. (1994) Occurrence of Bacillus species on evergreen oak leaves. FEMS Microbiol. Ecol. 14, 331-342 https://doi.org/10.1111/j.1574-6941.1994.tb00118.x
  5. Chastagner, G. A. and Riley, K. (1990) Occurrence and control of benzimidazole and dicarboximide resistant Botrytis spp. on bulb crops in Western Washington and Oregon. Acta Hort. 266, 437-445
  6. Chernin, L., Ismailov, Z., Haran, S. and Chet, I. (1995) Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl. Environ. Microbiol. 61, 1720-1726
  7. Chiou, A. L. and Wu, W. S. (2001) Isolation, identification and evaluation of bacterial antagonists against Botrytis elliptica on lily. J. Phytopathol. 149, 319-324 https://doi.org/10.1046/j.1439-0434.2001.00627.x
  8. Cohen-Kupiec, R. and Chet, I. (1998) The molecular biology of chitin digestion. Curr. Opin. Biotechnol. 9, 270-277 https://doi.org/10.1016/S0958-1669(98)80058-X
  9. Doss, R. P., Chastagner, G. A. and Riley, K. L. (1984) Techniques for inoculum production and inoculation of lily leaves with Botrytis elliptica. Plant Dis. 68, 854-856 https://doi.org/10.1094/PD-69-854
  10. Elad, Y. (1996) Mechanisms involved in the biological control of Botrytis cinerea incited diseases. Eur. J. Plant Pathol. 102, 719- 732 https://doi.org/10.1007/BF01877146
  11. Emmert, E. A. B. and Handelsman, J. (1999) Biocontrol of plant disease: a (Gram-) positive perspective. FEMS Microbiol. Lett. 171, 1-9 https://doi.org/10.1111/j.1574-6968.1999.tb13405.x
  12. Felse, P. A. and Panda, T. (1999) Regulation and cloning of microbial chitinase genes. Appl. Microbiol. Biotechnol. 51, 141- 151 https://doi.org/10.1007/s002530051374
  13. Flach, J., Pilet, P. E. and Jollès, P. (1992) What's new in chitinase research? Experientia 48, 701-716 https://doi.org/10.1007/BF02124285
  14. Freeman, S., Minzm O., Kolesnik, I., Barbul, O., Zveibil, A., Maymon, M., Nitzani, Y., Kirshner, B., Rav-David, D., Bilu, A., Dag, A., Shafir, S. and Elad, Y. (2004) Trichoderma biocontrol of Colletotrichum acutatum and Botrytis cinerea and survival in strawberry. Eur. J. Plant Pathol. 110, 361-370 https://doi.org/10.1023/B:EJPP.0000021057.93305.d9
  15. Gooday, G.. W. (1990) The ecology of chitin degradation; in Advances in Microbial Ecology, Marshall, K. C. (ed.), pp. 387- 430, Plenum Press, New York, USA
  16. Gould, A. B., Kobayashi, D. Y. and Bergen, M. S. (1996) Identification of bacteria for biological control of Botrytis cinerea on petunia using a petal disk assay. Plant Dis. 80, 1029-1033 https://doi.org/10.1094/PD-80-1029
  17. Graham, L. S. and Sticklen, M. B. (1994) Plant chitinases. Can. J. Bot. 72, 1057-1083 https://doi.org/10.1139/b94-132
  18. Henrissat, B. and Bairoch A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 293, 781-788
  19. Hsieh, T. F. and Huang, J. W. (1998) Factors affecting disease development of Botrytis leaf blight of lily caused by Botrytis elliptica. Plant Pathol. Bull. 40, 227-240
  20. Huang, C. J. and Chen, C. Y. (2004) Gene cloning and biochemical characterization of chitinase CH from Bacillus cereus 28-9. Ann. Microbiol. 54, 289-297
  21. Keim, P., Kalif, A., Schupp, J., Hill, K., Travis, S. E., Richmond, K., Adair, D. M., Hugh-Jones, M., Kuske, C. R. and Jackson, P. (1997) Molecular evolution and diversity in Bacillus anthracis as detected by amplified fragment length polymorphism markers. J. Bacteriol. 179, 818-824
  22. Kobayashi, D. Y., Reedy, R. M., Bick, J. A. and Oudemans, P. V. (2002) Characterization of a chitinase gene from Stenotrophomonas maltophilia strain 34S1 and its involvement in biological control. Appl. Environ. Microbiol. 68, 1047-1054 https://doi.org/10.1128/AEM.68.3.1047-1054.2002
  23. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680- 685 https://doi.org/10.1038/227680a0
  24. Mabuchi, N. and Araki, Y. (2001) Cloning and sequencing of two genes encoding chitinases A and B from Bacillus cereus CH. Can. J. Microbiol. 47, 895-902 https://doi.org/10.1139/cjm-47-10-895
  25. Mabuchi, N., Hashizume, I. and Araki, Y. (2000) Characterization of chitinases excreted by Bacillus cereus CH. Can. J. Microbiol. 46, 370-375 https://doi.org/10.1139/cjm-46-4-370
  26. Manoil, C. and Beckwith, J. (1986) A genetic approach to analyzing membrane protein topology. Science 233, 1403-1408 https://doi.org/10.1126/science.3529391
  27. Martinez, C., Michaud, M., Belanger, R. R. and Tweddell, R. J. (2002) Identification of soils suppressive against Helminthosporium solani, the causal agent of potato silver scurf. Soil Biol. Biochem. 34, 1861-1868 https://doi.org/10.1016/S0038-0717(02)00199-2
  28. Migheli, Q., Aloi, C. and Gullino, M. L. (1990) Resistance of Botrytis elliptica to fungicides. Acta Hort. 266, 429-436
  29. Perlman, D. and Halvorson, H. O. (1983) A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. J. Mol. Biol. 167, 391-409 https://doi.org/10.1016/S0022-2836(83)80341-6
  30. Perrakis, A., Tews, I., Dauter, Z., Oppenheim, A. B., Chet, I., Wilson, K. S. and Vorgias, C. E. (1994) Crystal structure of a bacterial chitinase at 2.3$\AA$ resolution. Structure 2, 1169-1180 https://doi.org/10.1016/S0969-2126(94)00119-7
  31. Pleban, S., Chernin, L. and Chet, I. (1997) Chitinolytic activity of an endophytic strain of Bacillus cereus. Lett. Appl. Microbiol. 25, 284-288 https://doi.org/10.1046/j.1472-765X.1997.00224.x
  32. Sietsma, J. H. and Wessels, J. G. H. (1979) Evidence for covalent linkages between chitin and $\beta$-glucan in a fungal wall. J. Gen. Microbiol. 114, 99-108 https://doi.org/10.1099/00221287-114-1-99
  33. Silo-Suh, L. A., Lethbridge, B. J., Raffel, S. J., He, H., Clardy, J. and Handelsman, J. (1994) Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl. Environ. Microbiol. 60, 2023-2030
  34. Tantimavanich, S., Pantuwatana, S., Bhumiratana, A. and Panbangred, W. (1998) Multiple chitinase enzymes from a single gene of Bacillus licheniformis TP-1. J. Ferment. Bioeng. 85, 259-265 https://doi.org/10.1016/S0922-338X(97)85672-3
  35. Thamthiankul, S., Suan-Ngay, S., Tantimavanich, S. and Panbangred, W. (2001) Chitinase from Bacillus thuringiensis subsp. pakistani. Appl. Microbiol. Biotechnol. 56, 395-401 https://doi.org/10.1007/s002530100630
  36. Trudel, J. and Asselin, A. (1989) Detection of chitinase activity after polyacrylamide gel electrophoresis. Anal. Biochem. 178, 362-366 https://doi.org/10.1016/0003-2697(89)90653-2
  37. Watanabe, T., Ito, Y., Yamada, T., Hashimoto, M., Sekine, S. and Tanaka, H. (1994) The roles of the C-terminal domain and type III domains of chitinase A1 from Bacillus circulans WL-12 in chitin degradation. J. Bacteriol. 176, 4465-4472
  38. Watanabe, T., Kobori, K., Miyashita, K., Fujii, T., Sakai, H., Uchida, M. and Tanaka, H. (1993) Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL-12 as essential residues for chitinase activity. J. Biol. Chem. 268, 18567-18572
  39. Watanabe, T., Oyanagi, W., Suzuki, K. and Tanaka, H. (1990a) Chitinase system of Bacillus circulans WL-12 and importance of chitinase A1 in chitin degradation. J. Bacteriol. 172, 4017- 4022
  40. Watanabe, T., Suzuki, K., Oyanagi, W., Ohnishi, K. and Tanaka, H. (1990b) Gene cloning of chitinase A1 from Bacillus circulans WL-12 revealed its evolutionary relationship to Serratia chitinase and to the type III homology units of fibronectin. J. Biol. Chem. 265, 15659-15665

Cited by

  1. Isolation of a Chitinolytic Bacillus licheniformis S213 Strain Exerting a Biological Control Against Phoma medicaginis Infection vol.175, pp.7, 2015, https://doi.org/10.1007/s12010-015-1520-7
  2. Native soil bacteria isolates in Mexico exhibit a promising antagonistic effect againstFusarium oxysporumf. sp.radicis-lycopersici 2013, https://doi.org/10.1002/jobm.201200128
  3. Characterization of chitinase secreted by Bacillus cereus strain CH2 and evaluation of its efficacy against Verticillium wilt of eggplant vol.53, pp.6, 2008, https://doi.org/10.1007/s10526-007-9144-7
  4. Defense gene expression in Sorghum bicolor against Macrophomina phaseolina in leaves and roots of susceptible and resistant cultivars vol.9, pp.1, 2014, https://doi.org/10.1080/17429145.2013.832425
  5. Diversity of culturable root-associated/endophytic bacteria and their chitinolytic and aflatoxin inhibition activity of peanut plant in China vol.29, pp.1, 2013, https://doi.org/10.1007/s11274-012-1135-x
  6. Characterization of chitinase-producingSerratiaandBacillusstrains isolated from insects vol.44, pp.3, 2014, https://doi.org/10.1111/1748-5967.12056
  7. Identification and transcriptional analysis of genes involved in Bacillus cereus-induced systemic resistance in Lilium vol.54, pp.4, 2010, https://doi.org/10.1007/s10535-010-0123-y
  8. Isolation and characterization of chitinolytic rhizobacteria for the management of Fusarium wilt in tomato vol.30, pp.12, 2011, https://doi.org/10.1016/j.cropro.2011.02.032
  9. Potentiality of Bacillus subtilis as biocontrol agent for management of anthracnose disease of chilli caused by Colletotrichum gloeosporioides OGC1 vol.4, pp.2, 2014, https://doi.org/10.1007/s13205-013-0134-4
  10. Biosynthesis and characterization of a thermostable, alkali-tolerant chitinase from Bacillus pumilus JUBCH08 displaying antagonism against phytopathogenic Fusarium oxysporum vol.6, pp.1, 2016, https://doi.org/10.1007/s13205-016-0406-x
  11. Medium optimization for chitinase production from Trichoderma virens using central composite design vol.14, pp.6, 2009, https://doi.org/10.1007/s12257-008-0127-z
  12. Cloning and characterization of a bifunctional glycosyl hydrolase from an antagonistic Pseudomonas putida strain P3(4) vol.52, pp.3, 2012, https://doi.org/10.1002/jobm.201100232
  13. A Novel Scaffold for Developing Specific or Broad-Spectrum Chitinase Inhibitors vol.56, pp.12, 2016, https://doi.org/10.1021/acs.jcim.6b00615
  14. Biological Control of Meloidogyne hapla Using an Antagonistic Bacterium vol.30, pp.3, 2014, https://doi.org/10.5423/PPJ.OA.02.2014.0013
  15. Expression of chitinase gene in BL21 pET system and investigating the biocatalystic performance of chitinase-loaded AlgSep nanocomposite beads vol.104, 2017, https://doi.org/10.1016/j.ijbiomac.2017.03.119
  16. Bacillus pumilus SG2 chitinases induced and regulated by chitin, show inhibitory activity against Fusarium graminearum and Bipolaris sorokiniana vol.38, pp.2, 2010, https://doi.org/10.1007/s12600-009-0078-8
  17. Bacillus species as versatile weapons for plant pathogens: a review vol.31, pp.3, 2017, https://doi.org/10.1080/13102818.2017.1286950
  18. Purification and characterization of a novel antifungal endo-type chitosanase from Anabaena fertilissima vol.62, pp.3, 2012, https://doi.org/10.1007/s13213-011-0350-2
  19. Bacillus thuringiensis beyond insect biocontrol: plant growth promotion and biosafety of polyvalent strains vol.57, pp.4, 2007, https://doi.org/10.1007/BF03175344
  20. Disease suppression and crop improvement in moong beans (Vigna radiata) through Pseudomonas and Burkholderia strains isolated from semi arid region of Rajasthan, India vol.55, pp.6, 2010, https://doi.org/10.1007/s10526-010-9292-z
  21. Isolation of Bacteria Associated with the King Oyster Mushroom,Pleurotus eryngii vol.36, pp.1, 2008, https://doi.org/10.4489/MYCO.2008.36.1.013
  22. A novel strain of Brevibacillus laterosporus produces chitinases that contribute to its biocontrol potential vol.97, pp.4, 2013, https://doi.org/10.1007/s00253-012-4019-y
  23. Rhizosphere: its structure, bacterial diversity and significance vol.13, pp.1, 2014, https://doi.org/10.1007/s11157-013-9317-z
  24. Biotechnological approaches to develop bacterial chitinases as a bioshield against fungal diseases of plants vol.30, pp.3, 2010, https://doi.org/10.3109/07388551.2010.487258
  25. Bacterial diversity and soil enzyme activity in diseased and disease free apple rhizosphere soils vol.61, pp.4, 2011, https://doi.org/10.1007/s13213-010-0193-2
  26. Natural occurrence ofBacillus thuringiensisandBacillus cereusin eukaryotic organisms: a case for symbiosis vol.18, pp.3, 2008, https://doi.org/10.1080/09583150801942334
  27. Antifungal chitinases from Bacillus pumilus SG2: preliminary report vol.26, pp.8, 2010, https://doi.org/10.1007/s11274-010-0318-6
  28. Construction of a Promoter-probe Vector for Bacillus thuringiensis: the Identification of cis-acting Elements of the chiA Locus vol.64, pp.5, 2012, https://doi.org/10.1007/s00284-012-0100-0
  29. Use of chitinolytic Bacillus atrophaeus strain S2BC-2 antagonistic to Fusarium spp. for control of rhizome rot of ginger vol.63, pp.3, 2013, https://doi.org/10.1007/s13213-012-0552-2
  30. Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L vol.68, pp.9, 2012, https://doi.org/10.1002/ps.3301
  31. Chitinases: in agriculture and human healthcare vol.34, pp.3, 2014, https://doi.org/10.3109/07388551.2013.790874
  32. Detection of enzymatic activity and partial sequence of a chitinase gene in Metschnikowia pulcherrima strain MACH1 used as post-harvest biocontrol agent vol.123, pp.2, 2009, https://doi.org/10.1007/s10658-008-9355-5
  33. Characterization of regulatory regions involved in the inducible expression of chiB in Bacillus thuringiensis vol.197, pp.1, 2015, https://doi.org/10.1007/s00203-014-1054-3
  34. Cloning, Expression and Characterization of Thermophilic and Alkalophilic N-acetylglucosaminidase from Streptomyces sp. NK52 for the Targeted Production of N-acetylglucosamine vol.83, pp.3, 2013, https://doi.org/10.1007/s40011-013-0158-x
  35. Solid-state cultivation of Bacillus thuringiensis R 176 with shrimp shells and rice straw as a substrate for chitinase production vol.63, pp.2, 2013, https://doi.org/10.1007/s13213-012-0488-6
  36. ANN and RSM based modelling for optimization of cell dry mass of Bacillus sp. strain B67 and its antifungal activity against Botrytis cinerea 2017, https://doi.org/10.1080/13102818.2017.1379359
  37. Purification and partial characterization of a 36-kDa chitinase from Bacillus thuringiensis subsp. colmeri, and its biocontrol potential vol.46, pp.3-4, 2010, https://doi.org/10.1016/j.enzmictec.2009.10.007
  38. Selection of a compatible biocontrol strain mixture based on co-cultivation to control rhizome rot of ginger vol.43, 2013, https://doi.org/10.1016/j.cropro.2012.08.012
  39. Physiological response of Bacillus cereus C1L-induced systemic resistance in lily against Botrytis leaf blight vol.134, pp.1, 2012, https://doi.org/10.1007/s10658-012-0013-6
  40. Bacillus thuringiensis and Bacillus weihenstephanensis Inhibit the Growth of Phytopathogenic Verticillium Species vol.7, 2017, https://doi.org/10.3389/fmicb.2016.02171
  41. Characterization of polyvalent and safeBacillus thuringiensisstrains with potential use for biocontrol vol.49, pp.3, 2009, https://doi.org/10.1002/jobm.200800182
  42. Efficacy of probenazole for control of southern corn leaf blight vol.36, pp.2, 2011, https://doi.org/10.1584/jpestics.G10-94
  43. Chitinase biotechnology: Production, purification, and application vol.15, pp.1, 2015, https://doi.org/10.1002/elsc.201400173
  44. Extracellular hydrolases of strain Bacillus sp. 739 and their involvement in the lysis of micromycete cell walls vol.76, pp.4, 2007, https://doi.org/10.1134/S0026261707040054
  45. Production and partial characterization of chitinase from a halotolerant Planococcus rifitoensis strain M2-26 vol.26, pp.6, 2010, https://doi.org/10.1007/s11274-009-0259-0
  46. Characterization of a Chitinase (Chit62) from Serratia marcescens B4A and Its Efficacy as a Bioshield Against Plant Fungal Pathogens vol.50, pp.9-10, 2012, https://doi.org/10.1007/s10528-012-9515-3