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A Novel Variant of Narrow-Spectrum Antifungal Bacterial Lipopeptides That Strongly Inhibit Ganoderma boninense

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Abstract

Bacterial antifungal cyclic lipopeptides (ACLs) have become a promising alternative to synthetic fungicide to control pathogenic fungi. Bacillus sp. is known to produce three families of ACL, namely iturin, surfactin, and fengycin. In this paper, we characterized the ACLs produced by B. methylotrophicus HC51 (referred as HC51) mainly regarding its composition and effectivity against fungal plant pathogen. HC51 culture was tested against various pathogenic fungi and the ACLs were extracted and analyzed using liquid chromatography–electrospray ionization mass spectrometry. HC51 showed strong antifungal activity against the plant pathogens Ganoderma sp. and Fusarium sp. Cell-free methanol extract of HC51 contains iturin A and various variants of fengycin. C16 fengycin A was present in four fractions which indicates it as a major component of ACL from HC51. Five variants of fengycin were detected, four of which had been previously reported. We found a novel C17 fengycin F that is characterized by a substitution of l-ornithine into lysine. Considering that l-ornithine is an important building block of fengycin, this substitution suggests the possibility of an alternative pathway for fengycin biosynthesis.

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References

  1. Ho C, Hashim K (1997) Usefulness of soil mounding treatments in prolonging productivity of prime-aged Ganoderma infected palms. Planter 73:239–244

    Google Scholar 

  2. Muhamad H, Zainol M, Sahid I, Seman IA (2012) Determination of hexaconazole in field samples of an oil palm plantation. Drug Test Anal 4:112–117. https://doi.org/10.1002/dta.1351

    Article  CAS  Google Scholar 

  3. Maznah Z, Halimah M, Ismail S, Idris AS (2015) Dissipation of the fungicide hexaconazole in oil palm plantation. Environ Sci Pollut Res 22:19648–19657. https://doi.org/10.1007/s11356-015-5178-z

    Article  CAS  Google Scholar 

  4. Kiss L (2003) A review of fungal antagonists of powdery mildews and their potential as biocontrol agents. Pest Manag Sci 59:475–483. https://doi.org/10.1002/ps.689

    Article  CAS  Google Scholar 

  5. van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483. https://doi.org/10.1146/annurev.phyto.36.1.453

    Article  Google Scholar 

  6. Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513. https://doi.org/10.1016/j.micres.2008.08.007

    Article  CAS  Google Scholar 

  7. Romero D, de Vicente A, Rakotoaly RH et al (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant-Microbe Interact 20:430–440. https://doi.org/10.1094/MPMI-20-4-0430

    Article  CAS  Google Scholar 

  8. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009

    Article  CAS  Google Scholar 

  9. Tao Y, Bie X, Lv F et al (2011) Antifungal activity and mechanism of fengycin in the presence and absence of commercial surfactin against Rhizopus stolonifer. J Microbiol 49:146–150. https://doi.org/10.1007/s12275-011-0171-9

    Article  CAS  Google Scholar 

  10. Pathak KV, Keharia H, Gupta K et al (2012) Lipopeptides from the banyan endophyte, Bacillus subtilis K1: mass spectrometric characterization of a library of fengycins. J Am Soc Mass Spectrom 23:1716–1728. https://doi.org/10.1007/s13361-012-0437-4

    Article  CAS  Google Scholar 

  11. Wang C, Hu X, Liu K et al (2016) Draft genome sequence of Bacillus methylotrophicus FKM10, a plant growth-promoting rhizobacterium isolated from apple rhizosphere. Genome Announc 4:e01739-15. https://doi.org/10.1128/genomeA.01739-15

    Article  Google Scholar 

  12. Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J et al (2017) Bacillus methylotrophicus M4-96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 1–13. https://doi.org/10.1007/s00709-017-1109-9

  13. Agustina D, Purnamasari MI, Suwanto A (2016) Development of specific antifungal compound for Ganoderma boninense. In: 9th Int. Conf. Plant Prot. Trop.—Healthy Crops Healthy World. Kuching, pp 125–128

  14. Vanittanakom N, Loeffler W, Koch U, Jung G (1986) Fengycin—a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J Antibiot (Tokyo) 39:888–901. https://doi.org/10.7164/antibiotics.39.888

    Article  CAS  Google Scholar 

  15. Kumar P, Dubey RC, Maheshwari DK (2012) Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol Res 167:493–499. https://doi.org/10.1016/j.micres.2012.05.002

    Article  CAS  Google Scholar 

  16. Landy M, Warren GH, Rosenman SB, Colio LG (1948) Bacillomycin: an antibiotic from Bacillus subtilis active against pathogenic fungi. Proc Soc Exp Biol Med 67:539–541. https://doi.org/10.3181/00379727-67-16367

    Article  CAS  Google Scholar 

  17. Sadfi N, Chérif M, Hajlaoui MR et al (2002) Isolation and partial purification of antifungal metabolites produced by Bacillus cereus. Ann Microbiol 52:323–337

    CAS  Google Scholar 

  18. Zhang S-M, Wang Y-X, Meng L-Q et al (2012) Isolation and characterization of antifungal lipopeptides produced by endophytic Bacillus amyloliquefaciens TF28. Afr J Microbiol Res 6:1747–1755. https://doi.org/10.5897/AJMR11.1025

    CAS  Google Scholar 

  19. Bernat P, Paraszkiewicz K, Siewiera P et al (2016) Lipid composition in a strain of Bacillus subtilis, a producer of iturin A lipopeptides that are active against uropathogenic bacteria. World J Microbiol Biotechnol 32:157. https://doi.org/10.1007/s11274-016-2126-0

    Article  Google Scholar 

  20. Vater J, Kablitz B, Wilde C et al (2002) Matrix-assisted laser desorption ionization-time of flight mass spectrometry of lipopeptide biosurfactants in whole cells and culture filtrates of Bacillus subtilis C-1 isolated from petroleum sludge. Appl Environ Microbiol 68:6210–6219. https://doi.org/10.1128/AEM.68.12.6210-6219.2002

    Article  CAS  Google Scholar 

  21. Esumi Y, Suzuki Y, Itoh Y et al (2003) SNA-60-367 components, new peptide enzyme inhibitors of aromatase: structure of the fatty acid side chain and amino acid sequence by mass spectrometry. J Antibiot (Tokyo) 56:716–720. https://doi.org/10.7164/antibiotics.56.716

    Article  CAS  Google Scholar 

  22. Bie X, Lu Z, Lu F (2009) Identification of fengycin homologues from Bacillus subtilis with ESI-MS/CID. J Microbiol Methods 79:272–278. https://doi.org/10.1016/j.mimet.2009.09.013

    Article  CAS  Google Scholar 

  23. Chen L, Wang N, Wang X et al (2010) Characterization of two anti-fungal lipopeptides produced by Bacillus amyloliquefaciens SH-B10. Bioresour Technol 101:8822–8827. https://doi.org/10.1016/j.biortech.2010.06.054

    Article  CAS  Google Scholar 

  24. Sang-Cheol L, Kim S-H, Park I-H et al (2010) Isolation, purification, and characterization of novel fengycin S from Bacillus amyloliquefaciens LSC04 degrading-crude oil. Biotechnol Bioprocess Eng 15:246–253. https://doi.org/10.1007/s12257-009-0037-8

    Article  Google Scholar 

  25. Li X-Y, Mao Z-C, Wang Y-H et al (2012) ESI LC-MS and MS/MS characterization of antifungal cyclic lipopeptides produced by Bacillus subtilis XF-1. J Mol Microbiol Biotechnol 22:83–93. https://doi.org/10.1159/000338530

    Article  Google Scholar 

  26. Susanto A, Sudharto PS, Purba RY (2005) Enhancing biological control of basal stem rot disease (Ganoderma boninense) in oil palm plantations. Mycopathologia 159:153–157. https://doi.org/10.1007/s11046-004-4438-0

    Article  CAS  Google Scholar 

  27. Islam MS, Ali M, Rahman MS (2012) In vitro studies on the fungicidal effect on Trichoderma species in tea plantation. Bangladesh J Agric Res 36:677–683. https://doi.org/10.3329/bjar.v36i4.11758

    Google Scholar 

  28. Balouiri M, Sadiki M, Ibnsouda SK (2016) Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 6:71–79. https://doi.org/10.1016/j.jpha.2015.11.005

    Article  Google Scholar 

  29. Meletiadis J, Mouton JW, Meis JFGM et al (2001) Colorimetric assay for antifungal susceptibility testing of Aspergillus species. J Clin Microbiol 39:3402–3408. https://doi.org/10.1128/JCM.39.9.3402-3408.2001

    Article  CAS  Google Scholar 

  30. Lin T-P, Chen C-L, Chang L-K et al (1999) Functional and transcriptional analyses of a fengycin synthetase gene, fenC, from Bacillus subtilis. J Bacteriol 181:5060–5067

    CAS  Google Scholar 

  31. Steller S, Vollenbroich D, Leenders F et al (1999) Structural and functional organization of the fengycin synthetase multienzyme system from Bacillus subtilis b213 and A1/3. Chem Biol 6:31–41. https://doi.org/10.1016/S1074-5521(99)80018-0

    Article  CAS  Google Scholar 

  32. C-Y W, Chen C-L, Lee Y-H et al (2007) Nonribosomal synthesis of fengycin on an enzyme complex formed by fengycin synthetases. J Biol Chem 282:5608–5616. https://doi.org/10.1074/jbc.M609726200

    Article  Google Scholar 

  33. Jemil N, Manresa A, Rabanal F et al (2017) Structural characterization and identification of cyclic lipopeptides produced by Bacillus methylotrophicus DCS1 strain. J Chromatogr B 1060:374–386. https://doi.org/10.1016/j.jchromb.2017.06.013

    Article  CAS  Google Scholar 

  34. Coutte F, Leclère V, Béchet M et al (2010) Effect of pps disruption and constitutive expression of srfA on surfactin productivity, spreading and antagonistic properties of Bacillus subtilis 168 derivatives. J Appl Microbiol 109:480–491. https://doi.org/10.1111/j.1365-2672.2010.04683.x

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank fellow PT Wilmar Benih Indonesia, Biotechnology R&D staffs Cahya Prihatna, and Maria Indah Purnamasari who have helped in the writing of this article.

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Correspondence to Antonius Suwanto.

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Pramudito, T.E., Agustina, D., Nguyen, T.K.N. et al. A Novel Variant of Narrow-Spectrum Antifungal Bacterial Lipopeptides That Strongly Inhibit Ganoderma boninense . Probiotics & Antimicro. Prot. 10, 110–117 (2018). https://doi.org/10.1007/s12602-017-9334-2

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