Study of endophytic Bacillus amyloliquefaciens CC09 and its antifungal cyclic lipopeptides

Cai Xun-Chao; Li Hui; Xue Ya-Rong; Liu Chang-Hong

doi:10.7324/JABB.2013.1101

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Abstract

Endophytic microbes are considered to be one of the most important bioactive compounds pool with a potential application in both pharmaceutical and agrichemical industries since the observation of taxol that could be synthesized by endophytic fungus Taxomyces andreanae. In this study, we reported an endophytic bacterium CC09, which was isolated from healthy Cinnamomum camphora leaves, exhibited a potential to produce antifungal metabolites inhibiting the growth of several phytopathogens such as Glomerella glycines, Rhizoctonia solani and Alternaria alternate. Based on 16S rRNA and rpoB genes analysis and physiological and biochemical assays, the strain CC09 was identified as Bacillus amyloliquefaciens. The antifungal constitutes in the culture filtrate of strain CC09 were predicted to be iturin family based on PCR amplification of specific genes including BmyC, ItuC, ItuD, ItuF and ItuR (encoding Iturin synthethases), FenD and FenE (encoding Fengency synthethases) and SrfC (encoding Surfactin synthethases), and confirmed by high performance liquid chromatography (HPLC). The broad antifungal spectra of the active constitutes in the metabolites indicated that the endophytic bacterium strain CC09 could be used as a potential biocontrol agent to control plant fungal diseases.

Keyword: Endophytic bacterium Bacillus amyloliquefaciens iturins antifungal activity.

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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3. Weyens N, Van der Lelie D, Taghavi S, Vangronsveld J. Phytoremediation: plant-endophyte partnerships take the challenge. Current Opinion in Biotechnology. 2009; 20:248-254. https://doi.org/10.1016/j.copbio.2009.02.012
4. Strobel G, Stierlea A, Stierle D. Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of pacific yew. Science. 1993; 260(9):214-216.
5. Zhu SM. Isolation and identification of endophytes in Ginkgo bilobaL. Journal of the graduates(in Chinese). 2011; 32:64-74.
6. Zhai YN, Guo H, Wei H, Zhan DJ, Yao SL, Hao H, Bie XM. Current State in Fermentation, Isolation, and Purification of Lipopeptide Antibiotics from Bacillussp. China Biotechnology. 2011; 31(11):114-122.
7. Toure Y, Ongena M, Jacques P, Guiro A, Thonart P. Role of lipopeptides produced by Bacillusgrey mould disease caused by Botrytis cinerea on apple. Journal of Applied Microbiology. 2004; 96: 1151-1160. https://doi.org/10.1111/j.1365-2672.2004.02252.x
8. Marc O, Philippe J. Bacilluslipopeptides:versatile weapons for plant disease biocontrol. Trends in Microbiology. 2008; 16(3):115-125. https://doi.org/10.1016/j.tim.2007.12.009
9. Deleu M, Paquot M, Nylander T. Fengycin interaction with lipid monolayers at the air-aqueous interface-implications for the effect of fengycin on biological membranes. Journal of Colloid and Interface Science. 2005; 283:358-365. https://doi.org/10.1016/j.jcis.2004.09.036
10. Chien HH, Mu TC, Lina H, Wen SC. Development of a novel PCR assay based on the gyrase B gene for species identification of Bacilluslicheniformis. Molecular and Cellular Probes. 2012; 25:215-217.
11. Krzysztofa N, Mariusz B, MichaÅ‚ O. Multicellular behaviour and production of a wide variety of toxic substances support usage of Bacillussubtilis as a powerful biocontrol agent. Acta Biochimica polonica. 2007; 54(3):495-508.
12. Liu CH, Zou WX, Lu H, Tan RX. Antifungal activity of Artimisia annua endophyte cultures against some phytopathogenic fungi. Journal of Biotechnology. 2001; 88:277-282. https://doi.org/10.1016/S0168-1656(01)00285-1
13. Liu CH, Chen X, Liu TT, Lian B, Gu Y, Caer V, Xue YR, Wang BT. Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its antifungal components. Applied Microbiology and Biotechnology. 2007; 76:459-466. https://doi.org/10.1007/s00253-007-1010-0
14. Li H, Wang X, Han M, Zhao Z, Wang M, Tang Q, Liu C, Kemp B, Gu Y, Shuang J. Endophytic Bacillussubtilis ZZ120 and its potential application in control of replant diseases. African Journal ofBiotechnology. 2012; 11(1):231-242.
15. Roberts MS, Nakamura LK, Cohan FM. Bacillusmojavensis sp. nov, distinguishable from Bacillussubtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition. International Journal of Systematic and Evolutionary Microbiology. 1994; 44:256-64.
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17. Sturz AV, Christie BR, Nowak J. Bacterial endophytes: potential role in developing sustainable system of crop production. Critical Reviews in Plant Sciences. 2000; 19:1-30. https://doi.org/10.1080/07352680091139169
18. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillusamyloliquefaciens FZB42. Nature Biotechnology. 2007; 25(9):1007-1014. https://doi.org/10.1038/nbt1325
19. Buchanan RE, Gibbons NE. Berger bacteria identification manual (eighth edition). science press. 1984; 752.
20. Dong XZ, Cai MY. Common bacteria identification system manual.science press. 2001.
21. Nakamura LK, Roberts MS, Cohan FM. Relationship of Bacillussubtilis clades associated with strains 168 and W23: a proposal for Bacillus subtilis subsp. subtilis subsp. nov. and Bacillussubtilis subsp. spizizenii subsp. nov. International Journal of Systematic Bacteriology. 1999; 49:1211-1215. https://doi.org/10.1099/00207713-49-3-1211
22. Roberts MS, Nakamura LK, Cohan FM. Bacillusmojavensis sp. Nov., distinguishable from Bacillussubtilis by sexual isolation, divergencein DNA sequence, and differences in fatty acid composition. International Journal of Systematic and Evolutionary Microbiology. 1994; 44:256-264.
23. Reller LB, Weinstein MP, Petti CA. Detection and identification of microorganisms by gene amplification and sequencing. Clinical Infectious Diseases. 2007; 44:1108-1114. https://doi.org/10.1086/512818
24. Janda JM, Abbott SL. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. Journal Clinical Microbiology. 2007; 45:2761-2764. https://doi.org/10.1128/JCM.01228-07
25. Palys T, Berger E, Mitrica I, Nakamura LK, Cohan FM. Proteincoding genes as molecular markers for ecologically distinct populations: the case of two Bacillusspecies. International Journal of Systematic and Evolutionary Microbiology. 2000; 50(3):1021-1028. https://doi.org/10.1099/00207713-50-3-1021
26. Rooney AP, Price NPJ, Ehrhardt C, Swezey JL, Bannan JD. Phylogeny and molecular taxonomy of the Bacillussubtilis species complex and description of Bacillussubtilis subsp. Inaquosorum subsp. nov. International Journal of Systematic and Evolutionary Microbiology. 2009; 59(10):2429-2436. https://doi.org/10.1099/ijs.0.009126-0
27. Fukumoto J. Studies on the production of bacterial amylase.I.Isolation of bacteria secreting potent amylases and their distribution. Journal of the Agricultural Chemical Society of Japan (in Japanese). 1943; 19: 487–503. https://doi.org/10.1271/nogeikagaku1924.19.7_487
28. Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B, Fickers P. Bacillusamyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microbial Cell Factories. 2009; 8:63. https://doi.org/10.1186/1475-2859-8-63
29. Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R. Genome analysis of Bacillusamyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. Journal of Biotechnology. 2009; 140: 27-37. https://doi.org/10.1016/j.jbiotec.2008.10.011
30. Asaka O, Shoda M. Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillussubtilis RB14. Applied Environmental Microbiology. 1996; 62:4081-4085.
31. Athukorala S.N.P., Fernando W.G.D., Rashid K.Y. Identification of antifungal antibiotics of Bacillus species isolated from different microhabitats using polymerase chain reaction and MALDI-TOF mass spectrometry. Canadian Journal of Microbiology. 2009;55:1021-1032. https://doi.org/10.1139/W09-067

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1. Compant S, Cle´ment C, Sessitsch A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, Xun-Chao et al. / Journal of Applied Biology & Biotechnology 1 (01); 2013:001-005 005colonization, mechanisms involved and prospects for utilization. Soil Biology and Biochemistry. 2010; 42:669-678. https://doi.org/10.1016/j.soilbio.2009.11.024

2. Barbara R, Thomas H. Living inside plants: bacterial endophytes.Current Opinion in Plant Biology. 2011; 4:435-453.

3. Weyens N, Van der Lelie D, Taghavi S, Vangronsveld J. Phytoremediation: plant-endophyte partnerships take the challenge. Current Opinion in Biotechnology. 2009; 20:248-254. https://doi.org/10.1016/j.copbio.2009.02.012

4. Strobel G, Stierlea A, Stierle D. Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of pacific yew. Science. 1993; 260(9):214-216.

5. Zhu SM. Isolation and identification of endophytes in Ginkgo bilobaL. Journal of the graduates(in Chinese). 2011; 32:64-74.

6. Zhai YN, Guo H, Wei H, Zhan DJ, Yao SL, Hao H, Bie XM. Current State in Fermentation, Isolation, and Purification of Lipopeptide Antibiotics from Bacillussp. China Biotechnology. 2011; 31(11):114-122.

7. Toure Y, Ongena M, Jacques P, Guiro A, Thonart P. Role of lipopeptides produced by Bacillusgrey mould disease caused by Botrytis cinerea on apple. Journal of Applied Microbiology. 2004; 96: 1151-1160. https://doi.org/10.1111/j.1365-2672.2004.02252.x

8. Marc O, Philippe J. Bacilluslipopeptides:versatile weapons for plant disease biocontrol. Trends in Microbiology. 2008; 16(3):115-125. https://doi.org/10.1016/j.tim.2007.12.009

9. Deleu M, Paquot M, Nylander T. Fengycin interaction with lipid monolayers at the air-aqueous interface-implications for the effect of fengycin on biological membranes. Journal of Colloid and Interface Science. 2005; 283:358-365. https://doi.org/10.1016/j.jcis.2004.09.036

10. Chien HH, Mu TC, Lina H, Wen SC. Development of a novel PCR assay based on the gyrase B gene for species identification of Bacilluslicheniformis. Molecular and Cellular Probes. 2012; 25:215-217.

11. Krzysztofa N, Mariusz B, MichaÅ‚ O. Multicellular behaviour and production of a wide variety of toxic substances support usage of Bacillussubtilis as a powerful biocontrol agent. Acta Biochimica polonica. 2007; 54(3):495-508.

12. Liu CH, Zou WX, Lu H, Tan RX. Antifungal activity of Artimisia annua endophyte cultures against some phytopathogenic fungi. Journal of Biotechnology. 2001; 88:277-282. https://doi.org/10.1016/S0168-1656(01)00285-1

13. Liu CH, Chen X, Liu TT, Lian B, Gu Y, Caer V, Xue YR, Wang BT. Study of the antifungal activity of Acinetobacter baumannii LCH001 in vitro and identification of its antifungal components. Applied Microbiology and Biotechnology. 2007; 76:459-466. https://doi.org/10.1007/s00253-007-1010-0

14. Li H, Wang X, Han M, Zhao Z, Wang M, Tang Q, Liu C, Kemp B, Gu Y, Shuang J. Endophytic Bacillussubtilis ZZ120 and its potential application in control of replant diseases. African Journal ofBiotechnology. 2012; 11(1):231-242.

15. Roberts MS, Nakamura LK, Cohan FM. Bacillusmojavensis sp. nov, distinguishable from Bacillussubtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition. International Journal of Systematic and Evolutionary Microbiology. 1994; 44:256-64.

16. Lodewyckx C, Vangronsfeld J, Porteous F, Moore ERB, Taghavi S, Mergeay M, Lelie D. Endophytic bacteria and their potential applications. Critical Reviews in Plant Sciences. 2002; 21:583-606. https://doi.org/10.1080/0735-260291044377

17. Sturz AV, Christie BR, Nowak J. Bacterial endophytes: potential role in developing sustainable system of crop production. Critical Reviews in Plant Sciences. 2000; 19:1-30. https://doi.org/10.1080/07352680091139169

18. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillusamyloliquefaciens FZB42. Nature Biotechnology. 2007; 25(9):1007-1014. https://doi.org/10.1038/nbt1325

19. Buchanan RE, Gibbons NE. Berger bacteria identification manual (eighth edition). science press. 1984; 752.

20. Dong XZ, Cai MY. Common bacteria identification system manual.science press. 2001.

21. Nakamura LK, Roberts MS, Cohan FM. Relationship of Bacillussubtilis clades associated with strains 168 and W23: a proposal for Bacillus subtilis subsp. subtilis subsp. nov. and Bacillussubtilis subsp. spizizenii subsp. nov. International Journal of Systematic Bacteriology. 1999; 49:1211-1215. https://doi.org/10.1099/00207713-49-3-1211

22. Roberts MS, Nakamura LK, Cohan FM. Bacillusmojavensis sp. Nov., distinguishable from Bacillussubtilis by sexual isolation, divergencein DNA sequence, and differences in fatty acid composition. International Journal of Systematic and Evolutionary Microbiology. 1994; 44:256-264.

23. Reller LB, Weinstein MP, Petti CA. Detection and identification of microorganisms by gene amplification and sequencing. Clinical Infectious Diseases. 2007; 44:1108-1114. https://doi.org/10.1086/512818

24. Janda JM, Abbott SL. 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. Journal Clinical Microbiology. 2007; 45:2761-2764. https://doi.org/10.1128/JCM.01228-07

25. Palys T, Berger E, Mitrica I, Nakamura LK, Cohan FM. Proteincoding genes as molecular markers for ecologically distinct populations: the case of two Bacillusspecies. International Journal of Systematic and Evolutionary Microbiology. 2000; 50(3):1021-1028. https://doi.org/10.1099/00207713-50-3-1021

26. Rooney AP, Price NPJ, Ehrhardt C, Swezey JL, Bannan JD. Phylogeny and molecular taxonomy of the Bacillussubtilis species complex and description of Bacillussubtilis subsp. Inaquosorum subsp. nov. International Journal of Systematic and Evolutionary Microbiology. 2009; 59(10):2429-2436. https://doi.org/10.1099/ijs.0.009126-0

27. Fukumoto J. Studies on the production of bacterial amylase.I.Isolation of bacteria secreting potent amylases and their distribution. Journal of the Agricultural Chemical Society of Japan (in Japanese). 1943; 19: 487–503. https://doi.org/10.1271/nogeikagaku1924.19.7_487

28. Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B, Fickers P. Bacillusamyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microbial Cell Factories. 2009; 8:63. https://doi.org/10.1186/1475-2859-8-63

29. Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, Piel J, Borriss R. Genome analysis of Bacillusamyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. Journal of Biotechnology. 2009; 140: 27-37. https://doi.org/10.1016/j.jbiotec.2008.10.011

30. Asaka O, Shoda M. Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillussubtilis RB14. Applied Environmental Microbiology. 1996; 62:4081-4085.

31. Athukorala S.N.P., Fernando W.G.D., Rashid K.Y. Identification of antifungal antibiotics of Bacillus species isolated from different microhabitats using polymerase chain reaction and MALDI-TOF mass spectrometry. Canadian Journal of Microbiology. 2009;55:1021-1032. https://doi.org/10.1139/W09-067

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