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References

  1. Al-Anbagi, R. A. and Fakhir E. Hameed. 2006. Effect of furfural on the germination and production of sclerotia of Sclerotinia sclerotiorum. AL-fath J. 25.
  2. Bartnicki-Garcia, S. 1968. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Ann. Rev. Microbiol. 22: 87-108.
    Pubmed CrossRef
  3. Becker, J. O. 1993. Control of soil-born pathogens with living bacteria and fungi: Status and outlook. Pesticide Sci. 37: 355-363.
    CrossRef
  4. Chun, J. and M. Goodfellow. 1995. A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int. J. Syst. Bacteriol. 45: 240-245.
    Pubmed CrossRef
  5. Dai, D. H., W. L. Hu, G. R. Huang, and W. Li. 2011. Purification and characterization of a novel extracellular chitinase from thermophilic Bacillus sp. Hu1. Afr. J. Biotechnol. 10:2476-2485.
  6. Fiedler, H. P., S. Worner, H. Zahner, H. P. Kaiser, W. K. Schierlein, and A. Muller. 1981. Metabolic products of microorganisms:Isolation and characterization of niphithricins A, B, and elaiophylin, antibiotics produced by Streptomyces violaceoniger. J. Antibiotics 34: 1107-1118.
    Pubmed CrossRef
  7. Forman, L. B., J. Postma, and J. A. Van Veen. 2003. Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8, a powerful antagonist of fungal disease of cucumber. Microbiol. Res. 158: 107-115.
    Pubmed CrossRef
  8. Getha, K. and S. Vikineswary. 2002. Antagonistic effects of Streptomyces violaceusniger strain G10 on Fusarium oxysporum f.sp. cubense race 4: Indirect evidence for the role of antibiosis in the antagonistic process. J. Ind. Microbiol. Biotechnol. 28:303-310.
    Pubmed CrossRef
  9. Handelsman, J. and E. V. Stabb. 1996. Biocontrol of soilborne plant pathogen. Plant Cell 8: 1855-1869.
    Pubmed PMC
  10. Holtzel, A., C. Kempter, J. G. Metzger, G. Jung, I. Groth, T. Fritz, and H. P. Fiedler. 1998. Spirofungin, a new antifungal antibiotic from Streptomyces violaceusniger Tu 4113. J. Antibiotics 51: 699-707.
    CrossRef
  11. Horváth, I. S., C. J. Franzén, J. Mohammad, M. J. Taherzadeh, C. Niklasson, and G. Lidén, 2003. Effects of furfural on the respiratory metabolism of Saccharomyces cerevisiae in glucoselimited chemostats. Appl. Environ. Microbiol. 4076-4086.
    Pubmed PMC
  12. Joo, G. J. 2005. Production of an anti-fungal substance for biological control of Phytophthora capsici causing Phytophthora blight in red-peppers by Streptomyces halstedii. Biotechnol. Lett. 27: 201-205.
    Pubmed CrossRef
  13. Klose, S. and M. A. Tabatabai. 2002. Response of amidohydrolases in soils to chloroform fumigation. J. Plant Nutr. Soil Sci. 165:125-132.
    CrossRef
  14. Klose, S. and M. A. Tabatabai. 1998. Urease activity of microbial biomass in soils. Soil Biol. Biochem. 31: 205-211.
    CrossRef
  15. Ko, H. S., R. D. Jin, H. B. Krishnan, S. B. Lee, and K. Y. Kim. 2009. Biocontrol ability of Lysobacter antibioticus HS124 against Phytophthora blight is mediated by the production of 4-hydrocyphenylacetic acid and several lytic enzymes. Curr. Microbiol. 59: 608-615.
    Pubmed CrossRef
  16. Ko, H. S., H. Tindwa, R. D. Jin, Y. S. Lee, S. H. Hong, H. N. Hyun, et al. 2011. Investigation of siderophore production and antifungal activity against Phytophthora capsici as related to iron (iii) nitrition by Lysobacter antibioticus HS124. Korean J. Soil Sci. Fertilizer 44: 650-656.
  17. Kokubun, T., J. B. Hrborne, J. Eagles, and P. G. Waterman. 1995. Dibenzofuran phytoalexins from the sapwood of Cotoneaster acutifolius and five related species. Phytochemistry 38: 57-60.
    CrossRef
  18. Kwon, C. S. and S. G. Lee. 2002. Occurrence and ecological characterization of red pepper anthracnose. Res. Plant Dis. 8:120-123.
    CrossRef
  19. Lazarova, G., V. Kostov, S. Zhelev, V. Ivanova, and T. Sokoloov. 1990. The effect of acetic acid and furfural on yeast growth. Acta Microbiol. Bulg. 25: 24-30.
    Pubmed
  20. Lingappa, Y. and J. L. Lockwood. 1962. Chitin media for selected isolation and culture of actinomycetes. Phytopathology 52: 317-323.
  21. Lloyd, A. B., R. L. Noveroske, and J. L. Lockwood. 1965. Lysis of fungal mycelium by Streptomyces spp. and their chitinase systems. Phytopathology 55: 871-875.
    Pubmed
  22. Mahadevan, B. and D. L. Crawford. 1997. Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108. Enzyme Microb. Technol. 20: 489-493.
    CrossRef
  23. Mayerhofer, H. J., R. T. Marshall, C. H. White, and M. Lu. 1972. Characterization of a heat-stable protease of Pseudomonas fluorescens P26. Appl. Microbiol. 25: 44-48.
  24. Obagwu, J. and L. Korsten. 2003. Intergrated control of citrus green and blue molds using Bacillus subtilis in combination with sodium bicarbonate of hot water. Postharvest Biol. Technol. 28: 187-194.
    CrossRef
  25. Palaniyandi, S. A., S. H. Yang, J. H. Cheng, L. Meng, and J. W. Suh. 2011. Biological control of anthracnose (Colletotrichum gloeosporioides) in yam by Streptomyces sp. MJM5763. J. Appl. Microbiol. 111: 443-455.
    Pubmed CrossRef
  26. Park, K. S. and C. H. Kim. 1992. Identification, distribution and etiological characteristics of anthracnose fungi of red pepper in Korea. Korean J. Plant Pathol. 8: 61-69.
  27. Prapagdeé, B., C. Kuekulvong, and S. Mongkolsuk. 2008. Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. Int. J. Biol. Sci. 4: 330-337.
    Pubmed PMC
  28. Sang, M. K., S. Chun, and K. D. Kim. 2008. Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol. Control 46: 424-433.
    CrossRef
  29. Soares, A. C. F., C. S. Sousa, M. S. Garrido, J. O. Perez, and N. S. de Almeida. 2006. Soil streptomycetes with in vitro activity against the yam pathogens Curvularia eragrostides and Colletotrichum gloeosporioides. Brazilian J. Microbiol. 37:456-461.
    CrossRef
  30. Trejo-Estrada, S. R., I. R. Sepulveda, and D. L. Crawford. 1998. In vitro and in vivo antagonism of Streptomyces violaceusniger YCED9 against fungal pathogens of turfgrass. World J. Microbiol. Biotechnol. 14: 865-872.
    CrossRef
  31. Yedidia, I., N. Benhamou, Y. Kapulnik, and I. Chet. 2000. Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol. Biochem. 38: 863-873.
    CrossRef
  32. Yoon, G. Y., Y. S. Lee, S. Y. Lee, R. D. Park, H. N. Hyun, Y. Nam, and K. Y. Kim. 2012. Effects on Meloidogyne incognita of chitinase, glucanase and a secondary metabolite from Streptomyces cacaoi GY525. Nematology 14: 175-184.
    CrossRef
  33. Zivkovi , S., S. Stojanovi , Z. Ivanovi , V. Gavrilovi , T. Popovi , and J. Balaž. 2010. Screening of antagonistic activity of microorganisms against Colletotrichum acutatum and Colletotrichum gloeosporioides. Arch. Biol. Sci. Belgrade 62:611-623.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2012; 22(10): 1359-1366

Published online October 28, 2012 https://doi.org/10.4014/jmb.1203.02056

Copyright © The Korean Society for Microbiology and Biotechnology.

Biocontrol of Anthracnose in Pepper Using Chitinase, β-1,3 Glucanase, and 2-Furancarboxaldehyde Produced by Streptomyces cavourensis SY224

So Youn Lee 1, Hamisi Tindwa 1, Yong Seong Lee 1, Kyaw Wai Naing 1, Seong Hyun Hong 1, Yi Nam 2 and Kil Yong Kim 1*

1Department of Agricultural Chemistry, Chonnam National University, Gwangju 500-757, Korea, 2Ansung Training Institute, National Agricultural Cooperative Federation, Ansung 456-824, Korea

Received: March 5, 2012; Accepted: May 22, 2012

Abstract

A strain of Streptomyces cavourensis subsp. cavourensis (coded
as SY224) antagonistic to Colletotrichum gloeosporioides
infecting pepper plants was isolated. SY224 produced
lytic enzymes such as chitinase, β-1,3-glucanase, lipase,
and protease in respective assays. To examine for antifungal
activity, the treatments amended with the nonsterilized
supernatant resulted in the highest growth inhibition rate
of about 92.9% and 87.4% at concentrations of 30% and
10%, respectively. However, the sterilized treatments
(autoclaved or chloroform treated) gave a lowered but
significant inhibitory effect of about 63.4% and 62.6% for
the 10% supernatant concentration, and 75.2% and 74.8%
for the of 30% supernatant concentration in the PDA
agar medium, respectively, indicative of the role of a nonprotein,
heat stable compound on the overall effect. This
antifungal compound, which inhibited spore germination
and altered hyphal morphology, was extracted by EtOAc
and purified by ODS, silica gel, Sephadex LH-20 column,
and HPLC, where an active fraction was confirmed to be
2-furancarboxaldehyde by GS-CI MS techniques. These
results suggested that SY224 had a high potential in the
biocontrol of anthracnose in pepper, mainly due to a
combined effect of lytic enzymes and a non-protein, heatstable
antifungal compound, 2-furancarboxaldehyde.

Keywords: Antifungal activity, β-1,3 glucanase, chitinase, 2-furancarboxaldehyde, Streptomyces cavourensis

References

  1. Al-Anbagi, R. A. and Fakhir E. Hameed. 2006. Effect of furfural on the germination and production of sclerotia of Sclerotinia sclerotiorum. AL-fath J. 25.
  2. Bartnicki-Garcia, S. 1968. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Ann. Rev. Microbiol. 22: 87-108.
    Pubmed CrossRef
  3. Becker, J. O. 1993. Control of soil-born pathogens with living bacteria and fungi: Status and outlook. Pesticide Sci. 37: 355-363.
    CrossRef
  4. Chun, J. and M. Goodfellow. 1995. A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int. J. Syst. Bacteriol. 45: 240-245.
    Pubmed CrossRef
  5. Dai, D. H., W. L. Hu, G. R. Huang, and W. Li. 2011. Purification and characterization of a novel extracellular chitinase from thermophilic Bacillus sp. Hu1. Afr. J. Biotechnol. 10:2476-2485.
  6. Fiedler, H. P., S. Worner, H. Zahner, H. P. Kaiser, W. K. Schierlein, and A. Muller. 1981. Metabolic products of microorganisms:Isolation and characterization of niphithricins A, B, and elaiophylin, antibiotics produced by Streptomyces violaceoniger. J. Antibiotics 34: 1107-1118.
    Pubmed CrossRef
  7. Forman, L. B., J. Postma, and J. A. Van Veen. 2003. Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8, a powerful antagonist of fungal disease of cucumber. Microbiol. Res. 158: 107-115.
    Pubmed CrossRef
  8. Getha, K. and S. Vikineswary. 2002. Antagonistic effects of Streptomyces violaceusniger strain G10 on Fusarium oxysporum f.sp. cubense race 4: Indirect evidence for the role of antibiosis in the antagonistic process. J. Ind. Microbiol. Biotechnol. 28:303-310.
    Pubmed CrossRef
  9. Handelsman, J. and E. V. Stabb. 1996. Biocontrol of soilborne plant pathogen. Plant Cell 8: 1855-1869.
    Pubmed KoreaMed
  10. Holtzel, A., C. Kempter, J. G. Metzger, G. Jung, I. Groth, T. Fritz, and H. P. Fiedler. 1998. Spirofungin, a new antifungal antibiotic from Streptomyces violaceusniger Tu 4113. J. Antibiotics 51: 699-707.
    CrossRef
  11. Horváth, I. S., C. J. Franzén, J. Mohammad, M. J. Taherzadeh, C. Niklasson, and G. Lidén, 2003. Effects of furfural on the respiratory metabolism of Saccharomyces cerevisiae in glucoselimited chemostats. Appl. Environ. Microbiol. 4076-4086.
    Pubmed KoreaMed
  12. Joo, G. J. 2005. Production of an anti-fungal substance for biological control of Phytophthora capsici causing Phytophthora blight in red-peppers by Streptomyces halstedii. Biotechnol. Lett. 27: 201-205.
    Pubmed CrossRef
  13. Klose, S. and M. A. Tabatabai. 2002. Response of amidohydrolases in soils to chloroform fumigation. J. Plant Nutr. Soil Sci. 165:125-132.
    CrossRef
  14. Klose, S. and M. A. Tabatabai. 1998. Urease activity of microbial biomass in soils. Soil Biol. Biochem. 31: 205-211.
    CrossRef
  15. Ko, H. S., R. D. Jin, H. B. Krishnan, S. B. Lee, and K. Y. Kim. 2009. Biocontrol ability of Lysobacter antibioticus HS124 against Phytophthora blight is mediated by the production of 4-hydrocyphenylacetic acid and several lytic enzymes. Curr. Microbiol. 59: 608-615.
    Pubmed CrossRef
  16. Ko, H. S., H. Tindwa, R. D. Jin, Y. S. Lee, S. H. Hong, H. N. Hyun, et al. 2011. Investigation of siderophore production and antifungal activity against Phytophthora capsici as related to iron (iii) nitrition by Lysobacter antibioticus HS124. Korean J. Soil Sci. Fertilizer 44: 650-656.
  17. Kokubun, T., J. B. Hrborne, J. Eagles, and P. G. Waterman. 1995. Dibenzofuran phytoalexins from the sapwood of Cotoneaster acutifolius and five related species. Phytochemistry 38: 57-60.
    CrossRef
  18. Kwon, C. S. and S. G. Lee. 2002. Occurrence and ecological characterization of red pepper anthracnose. Res. Plant Dis. 8:120-123.
    CrossRef
  19. Lazarova, G., V. Kostov, S. Zhelev, V. Ivanova, and T. Sokoloov. 1990. The effect of acetic acid and furfural on yeast growth. Acta Microbiol. Bulg. 25: 24-30.
    Pubmed
  20. Lingappa, Y. and J. L. Lockwood. 1962. Chitin media for selected isolation and culture of actinomycetes. Phytopathology 52: 317-323.
  21. Lloyd, A. B., R. L. Noveroske, and J. L. Lockwood. 1965. Lysis of fungal mycelium by Streptomyces spp. and their chitinase systems. Phytopathology 55: 871-875.
    Pubmed
  22. Mahadevan, B. and D. L. Crawford. 1997. Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108. Enzyme Microb. Technol. 20: 489-493.
    CrossRef
  23. Mayerhofer, H. J., R. T. Marshall, C. H. White, and M. Lu. 1972. Characterization of a heat-stable protease of Pseudomonas fluorescens P26. Appl. Microbiol. 25: 44-48.
  24. Obagwu, J. and L. Korsten. 2003. Intergrated control of citrus green and blue molds using Bacillus subtilis in combination with sodium bicarbonate of hot water. Postharvest Biol. Technol. 28: 187-194.
    CrossRef
  25. Palaniyandi, S. A., S. H. Yang, J. H. Cheng, L. Meng, and J. W. Suh. 2011. Biological control of anthracnose (Colletotrichum gloeosporioides) in yam by Streptomyces sp. MJM5763. J. Appl. Microbiol. 111: 443-455.
    Pubmed CrossRef
  26. Park, K. S. and C. H. Kim. 1992. Identification, distribution and etiological characteristics of anthracnose fungi of red pepper in Korea. Korean J. Plant Pathol. 8: 61-69.
  27. Prapagdeé, B., C. Kuekulvong, and S. Mongkolsuk. 2008. Antifungal potential of extracellular metabolites produced by Streptomyces hygroscopicus against phytopathogenic fungi. Int. J. Biol. Sci. 4: 330-337.
    Pubmed KoreaMed
  28. Sang, M. K., S. Chun, and K. D. Kim. 2008. Biological control of Phytophthora blight of pepper by antagonistic rhizobacteria selected from a sequential screening procedure. Biol. Control 46: 424-433.
    CrossRef
  29. Soares, A. C. F., C. S. Sousa, M. S. Garrido, J. O. Perez, and N. S. de Almeida. 2006. Soil streptomycetes with in vitro activity against the yam pathogens Curvularia eragrostides and Colletotrichum gloeosporioides. Brazilian J. Microbiol. 37:456-461.
    CrossRef
  30. Trejo-Estrada, S. R., I. R. Sepulveda, and D. L. Crawford. 1998. In vitro and in vivo antagonism of Streptomyces violaceusniger YCED9 against fungal pathogens of turfgrass. World J. Microbiol. Biotechnol. 14: 865-872.
    CrossRef
  31. Yedidia, I., N. Benhamou, Y. Kapulnik, and I. Chet. 2000. Induction and accumulation of PR proteins activity during early stages of root colonization by the mycoparasite Trichoderma harzianum strain T-203. Plant Physiol. Biochem. 38: 863-873.
    CrossRef
  32. Yoon, G. Y., Y. S. Lee, S. Y. Lee, R. D. Park, H. N. Hyun, Y. Nam, and K. Y. Kim. 2012. Effects on Meloidogyne incognita of chitinase, glucanase and a secondary metabolite from Streptomyces cacaoi GY525. Nematology 14: 175-184.
    CrossRef
  33. Zivkovi , S., S. Stojanovi , Z. Ivanovi , V. Gavrilovi , T. Popovi , and J. Balaž. 2010. Screening of antagonistic activity of microorganisms against Colletotrichum acutatum and Colletotrichum gloeosporioides. Arch. Biol. Sci. Belgrade 62:611-623.
    CrossRef