Lipopeptides, a novel protein, and volatile compounds contribute to the antifungal activity of the biocontrol agent Bacillus atrophaeus CAB-1

Applied Microbiology and Biotechnology

Volumn 97, Issue 21, 2013, Pages 9525-9534

  Zhang, Xiaoyun ^a   Li, Baoqing ^a   Wang, Ye ^b   Guo, Qinggang ^a   Lu, Xiuyun ^a   Li, Shezeng ^a   Ma, Ping ^a  

^a AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Antifungal protein; Bacillus atrophaeus; Lipopeptides; Volatile compound

Indexed keywords

ANTAGONISTIC ACTIVITY; ANTIFUNGAL PROTEIN; BACILLUS ATROPHAEUS; LIPOPEPTIDES; MATRIX-ASSISTED LASER DESORPTION IONIZATION; SPHAEROTHECA FULIGINEA; TIME OF FLIGHT MASS SPECTROMETRY; VOLATILE COMPOUNDS;

ANTIFUNGAL AGENTS; BACTERIOLOGY; BIOCONTROL; MASS SPECTROMETRY; PATHOGENS; POLYACRYLATES; PROTEINS; VOLATILE ORGANIC COMPOUNDS;

FUNGI;

1 METHYLDODECYLAMINE; 2 HEXANAMINE, 5 METHYL AMINE; 2 METHYLAMINOMETHYL 1,3 DIOXOLANE; 2 OCTANAMINE; 2,3 DIMETHOXYBENZAMIDE; 3 BUTEN 2 ONE,4 (2,5,6,6 TETRAMETHYL 1 CYCLOHEXEN 1 YL) KETONE; ALCOHOL DERIVATIVE; ALDEHYDE DERIVATIVE; ALKANE DERIVATIVE; AMIDE; AMINE; ANTIFUNGAL AGENT; BACILLUS ATROPHAEUS CAB 1; BENZAMIDE; CYCLOBUTANOL; CYCLOPROPYL CARBINOL; DIMETHYLAMINE; ERYTHRITOL; HEXADECANE; ISOPHYTOL; KETONE DERIVATIVE; LIPOPEPTIDE; N, N DIMETHYL METHANESULFONAMIDE; O ANISALDEHYDE; PHENOL DERIVATIVE; PHENOL, 2,4 BIS(1,1 DIMETHYLETHYL); PHENOL, 2,5 BIS(1,1 DIMETHYLETHYL); PROPANAMIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VOLATILE AGENT;

ALKANE; BIOCONTROL AGENT; DESORPTION; DISEASE CONTROL; IONIZATION; MASS SPECTROMETRY; PATHOGEN; PEPTIDE; PROTEIN;

AMINO ACID SEQUENCE; ANTIFUNGAL ACTIVITY; ARTICLE; BACILLUS ATROPHAEUS; BIOLOGICAL CONTROL AGENT; BOTRYTIS CINEREA; CONTROLLED STUDY; CUCUMBER; DISEASE SEVERITY; DRUG EFFICACY; GREENHOUSE; IN VITRO STUDY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; MYCELIAL GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DISEASE CONTROL; POWDERY MILDEW;

BACILLI (CLASS); BACILLUS ATROPHAEUS; BOTRYOTINIA FUCKELIANA; CUCUMIS SATIVUS; ERYSIPHALES; LYCOPERSICON ESCULENTUM; PODOSPHAERA FULIGINEA;

ANTIBIOSIS; ASCOMYCOTA; BACILLUS; BACTERIAL PROTEINS; CUCUMIS SATIVUS; LIPOPEPTIDES; MICROBIAL SENSITIVITY TESTS; PLANT DISEASES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VOLATILE ORGANIC COMPOUNDS;

EID: 84885961419     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5198-x     Document Type: Article

References (39)

1. Alvarez F, Castro M, Principe A, Borioli G, Fischer S, Mori G, Jofre E (2012) The plant-associated Bacillus amyloliquefaciens strains MEP218 and ARP23 capable of producing the cyclic lipopeptides iturin or surfactin and fengycin are effective in biocontrol of sclerotinia stem rot disease. J Appl Microbiol 112:159-174. doi: 10.1111/j.1365-2672.2011.05182.x
2. Andersen RA, Hamilton-Kemp TR, Hildebrand DF, McCracken C, Collins RW, Fleming PD (1994) Structure-antifungal activity relationships among volatile C-6 and C-9 aliphatic-aldehydes, ketones, and alcohols. J Agric Food Chem 42:1563-1568. doi: 10.1021/jf00043a033
3. Arrebola E, Sivakumar D, Korsten L (2010) Effect of volatile compounds produced by Bacillus strains on postharvest decay in citrus. Biol Control 53:122-128. doi: 10.1016/j.biocontrol.2009.11.010
4. Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Margesin R, Maerk TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 74:2179-2186. doi: 10.1128/AEM.02069-07
5. Chaurasia B, Pandey A, Palni LM, Trivedi P, Kumar B, Colvin N (2005) Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiol Res 160:75-81. doi: 10.1016/j.micres.2004.09.013
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. doi: 10.1016/j.micres.2008.08.007
7. Dunlap CA, Schisler DA, Price NP, Vaughn SF (2011) Cyclic lipopeptide profile of three Bacillus subtilis strains; antagonists of Fusarium head blight. J Microbiol 49:603-609. doi: 10.1007/s12275-011-1044-y
8. Farag MA, Ryu C, Sumner LW, Pare PW (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262-2268. doi: 10.1016/j.phytochem.2006.07.021
9. Fernando W, Ramarathnam R, Krishnamoorthy A, Savchuk S (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955-964. doi: 10.1016/j.soilbio.2004.10.021
10. Guetsky R, Shtienberg D, Elad Y, Dinoor A (2001) Combining biocontrol agents to reduce the variability of biological control. Phytopathology 91:621-627
11. Hu LB, Shi ZQ, Zhang T, Yang ZM (2007) Fengycin antibiotics isolated from B-FS01 culture inhibit the growth of Fusarium moniliforme Sheldon ATCC 38932. FEMS Microbiol Lett 272:91-98. doi: 10.1111/j.1574-6968.2007.00743.x
12. Huang CJ, Chen CY (2008) Synergistic interactions between chitinase ChicCW and fungicides against plant fungal pathogens. J Microbiol Biotech 18:784-787
13. Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351-360. doi: 10.1007/s00203-006-0199-0
14. Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001-1012. doi: 10.1007/s00253-008-1760-3
15. Kavitha S, Senthilkumar S, Gnanamanickam S, Inayathullah M, Jayakumar R (2005) Isolation and partial characterization of antifungal protein from Bacillus polymyxa strain VLB16. Process Biochem 40:3236-3243. doi: 10.1016/j.procbio.2005.03.060
16. Kracht M, Rokos H, Ozel M, Kowall M, Pauli G, Vater J (1999) Antiviral and hemolytic activities of surfactin isoforms and their methyl ester derivatives. J Antibiot 52:613-619
17. Li J, Yang Q, Zhao LH, Zhang SM, Wang YX, Zhao XY (2009) Purification and characterization of a novel antifungal protein from Bacillus subtilis strain B29. J Zhejiang Univ Sci B 10:264-272. doi: 10.1631/jzus.B0820341
18. Li BQ, Lu XY, Guo QG, Qian CD, Li SZ, Ma P (2010a) Isolation and identification of lipopeptides and volatile compounds produced by Bacillus subtilis strain BAB-1. Scientia Agricultura Sinica 43:3547-3554
19. Li ZJ, Li BQ, Lu XY, Qian CD, Guo QG, Li SZ, Ma P (2010b) Research on the producing condition and stability of antifungal substance from biocontrol bacterium strain CAB-1. J Anhui Agric Sci 38(11):5700-5702,5777
20. Liu WW, Zhao LJ, Wang C, Mu W, Liu F (2009) Bioactive evaluation and application of antifungal volatiles generated by five soil bacteria. Acta Phytophy Sinica 36:97-105
21. Liu B, Huang LL, Buchenauer H, Kang ZS (2010) Isolation and partial characterization of an antifungal protein from the endophytic Bacillus subtilis strain EDR4. Pestic Biochem Physiol 98:305-311. doi: 10.1016/j.pestbp.2010.07. 001
22. Magetdana R, Thimon L, Peypoux F, Ptak M (1992) Surfactin/iturin A interactions may explain the Synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74:1047-1051. doi: 10.1016/0300-9084(92)90002- V
23. Malfanova N, Franzil L, Lugtenberg B, Chebotar V, Ongena M (2012) Cyclic lipopeptide profile of the plant-beneficial endophytic bacterium Bacillus subtilis HC8. Arch Microbiol 194:893-899. doi: 10.1007/s00203-012-0823-0
24. Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115-125. doi: 10.1016/j.tim.2007. 12.009
25. Ongena M, Jacques P, Toure Y, Destain J, Jabrane A, Thonart P (2005) Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Appl Microbiol Biotechnol 69:29-38. doi: 10.1007/s00253-005-1940-3
26. Pathak KV, Keharia H, Gupta K, Thakur SS, Balaram P (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. doi: 10.1007/s13361-012-0437-4
27. Perez-Garcia A, Romero D, de Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotechnol 22:187-193. doi: 10.1016/j.copbio.2010.12.003
28. Peypoux F, Bonmatin J, Wallach J (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51:553-563
29. Romero D, de Vicente A, Rakotoaly RH, Dufour SE, Veening J, Arrebola E, Cazorla FM, Kuipers OP, Paquot M, Perez-Garcia A (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. doi: 10.1094/MPMI-20-4-0430
30. Ryu C, Farag M, Hu C, Reddy M, Wei H, Pare P, Kloepper J (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100:4927-4932. doi: 10.1073/pnas.0730845100
31. Ryu C, Farag M, Hu C, Reddy M, Kloepper J, Pare P (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017-1026. doi: 10.1104/pp. 103.026583
32. Schneider J, Taraz K, Budzikiewicz H, Deleu M, Thonart P, Jacques P (1999) The structure of two fengycins from Bacillus subtilis S499. Z Naturforsch C 54c:859-866
33. Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814-842. doi: 10.1039/b507392h
34. Shi L, Guo QG, Li BQ, Lu XY, Li SZ, Ma P (2013) Screening and identification of an antifungal chitinolvtic bacterium and its chitinase encoding gene cloning and prokaryotic expressiong. Acta Phytophy Sinica (in press)
35. Stein T (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56:845-857. doi: 10.1111/j.1365-2958.2005. 04587.x
36. Vanittanakom N, Loeffler W, Koch U, Jung G (1986) Fengycin- a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29-3. J Antibiot 39:888-901
37. Wan M, Li G, Zhang J, Jiang D, Huang H (2008) Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biolo Control 46:552-559. doi: 10.1016/j.biocontrol.2008.05.015
38. Wong JH, Hao J, Cao Z, Qiao M, Xu H, Bai Y, Ng TB (2008) An antifungal protein from Bacillus amyloliquefaciens. J Appl Microbiol 105:1888-1898. doi: 10.1111/j.1365-2672.2008.03917.x
39. Zhao X, Zhao X, Wei Y, Shang Q, Liu Z (2013) Isolation and identification of a novel antifungal protein from a rhizobacterium Bacillus subtilis Strain F3. J Phytopathol 161:43-48. doi: 10.1111/jph.12015