Journal of Biological Control

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Metabolome heterogeneity in the isolates of entomopathogenic fungus, Beauveria bassiana (Balsamo) Vuillemin


Affiliations
1 Department of Agricultural Entomology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India
2 Department of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India
3 Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India
 

Entomopathogenic fungi are known to produce a multitude of low molecular weight secondary metabolites involved in different biological processes including fungal development, intercellular communication and interaction with other organisms in complex niches. In the present investigation, heterogeneity in metabolome profile of three isolates of Beauveria bassiana viz., MH590235 (TM), MK918495 (BR) and KX263275 (BbI8) were analyzed through GC-MS. Distinct differences in metabolite profile of the isolates were observed. A total of 63 metabolites were detected from all the isolates combined. Metabolites, 5-Oxotetrahydrofuran-2-carboxylic acid and undecane were found to be specific to BR isolate. Macrocyclic gamma lactones were detected in culture filtrates of BR and BbI8, oleic acid and hexadecanoic acid in TM and BR. An insecticidal compound, levoglucos an was detected in all the fungal isolates. Among the isolates, TM revealed higher variability in the metabolite production through PCA analysis. The metabolome of TM isolate contained compounds having several biological functions, viz., insecticidal and antimicrobial activity, lipid and fatty acid metabolisms and virulence enhancing factors.


Keywords

Beauveria bassiana, Biological Functions, GC-MS, Metabolome Heterogeneity, PCA Analysis.
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  • Amiri-Besheli B, Khambay B, Cameron S, Deadman ML, Butt T.M. 2000. Inter- and intra-specific variation in destruxin production by insect pathogenic Metarhizium spp., and its significance to pathogenesis. Mycol Res. 104: 447-452. https://doi.org/10.1017/S095375629900146X https://doi.org/10.1017/S095375629900146X

  • Bernabé M, Salvachúa D, Jiménez-Barbero J, Leal JA, Prieto A. 2011. Structures of wall heterogalactomannans isolated from three genera of entomopathogenic fungi. Fungal Biol. 115(9): 862-870. https://doi.org/10.1016/j.funbio.2011.06.015 https://doi.org/10.1016/j.funbio.2011.06.015 PMid:21872183

  • Brakhage AA. 2013 Regulation of fungal secondary metabolism. Nat Rev Microbiol. 11(1):21-32. https://doi.org/10.1038/nrmicro2916 https://doi.org/10.1038/nrmicro2916 PMid:23178386

  • Brennan PJ, Griffin PF, Lösel DM, Tyrrell D. 1975. The lipids of fungi. Prog Chem Fats Lipids 14: 49-89. https://doi.org/10.1016/0079-6832(75)90002-6

  • Butt TM, Jackson CW, Magan N. 2001. Fungi as Biocontrol Agents: Potential, Progress and Problems. CAB International, Wallingford. https://doi.org/10.1079/9780851993560.0000

  • deBekker C, Smith PB, Patterson AD, Hughes DP. 2013. Metabolomics reveals the heterogeneous secretome of two entomopathogenic fungi to ex vivo cultured insect tissues. PLoS ONE 8(8): e70609. https://doi.org/10.1371/journal.pone.0070609 PMid:23940603 PMCid:PMC3734240

  • Domon K, Keiji T, Yutaka O, Junichiro B, Kei K, Akira W, Masaaki K, Takeshi M, Seisuke I. 2018. “Alkyl phenyl sulfide derivative and pest control agent.” U.S. Patent Application 10/023,532, filed July 17, 2018.

  • Douglas CM. 2001. Fungal β (1, 3)-D-glucan synthesis. Sabouraudia 39(1): 55-66. https://doi.org/10.1080/ mmy.39.1.55.66 https://doi.org/10.1080/mmy.39.1.55.66 PMid:11800269

  • Gowri PM, Haribabu K, Kishore H, Manjusha O, Biswas S, Murty USN. 2011. Microbial transformation of(+)heraclenin by Aspergillus niger and evaluation of its antiplasmodial and antimicrobial activities. Current Sci. 100(11):1706-1711.

  • Hölldobler B, Wilson EO. 1990. The Ants. Harvard University Press, US. https://doi.org/10.1007/978-3-662-10306-7 PMid:24263721

  • Hyun SH, Lee SY, Sung GH, Kim SH, Choi HK. 2013. Metabolic Profiles and Free Radical Scavenging Activity of Cordyceps bassiana Fruiting Bodies According to Developmental Stage. PLoS ONE. 8(9): e73065. https://doi.org/10.1371/journal.pone.0073065 PMid:24058459 PMCid:PMC3772819

  • Retrieved from: https://pubchem.ncbi.nlm.nih.gov/ compound/Digitoxin

  • Kadowaki M, Godoy M, Kumagai P, Costa-Filho A, Mort A, Prade R, Polikarpov I. 2018. Characterization of a new glyoxal oxidase from the thermophilic fungus Myceliophthora thermophila M77: hydrogen peroxide production retained in 5-hydroxymethylfurfural oxidation. Catalysts 8(10): 476. https://doi.org/10.3390/catal8100476.

  • Keller NP. 2015. Translating biosynthetic gene clusters into fungal armor and weaponry. Nat Chem Biol.

  • (9):671-677. https://doi.org/10.1038/nchembio.1897 PMid:26284674 PMCid:PMC4682562

  • Kershaw MJ, Moorhouse ER, Bateman RP, Reynolds SE, Charnley AK. 1999. The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insect. J Invertebr Pathol. 74: 213-223. https://doi.org/10.1006/jipa.1999.4884 PMid:10534408

  • Liu H, Zhao X, Guo M, Liu H, Zheng Z. 2015. Growth and metabolism of Beauveria bassiana spores and mycelia. BMC Microbiology 15(1): 267. https://doi.org/10.1186/s12866-015-0592-4 PMid:26581712 PMCid:PMC4652391

  • Liu L, Liu S, Chen X, Guo, L, Che Y. 2009. Pestalofones A-E, bioactive cyclohexanone derivatives from the plant endophytic fungus Pestalotiopsis fici. Bioorg Med Chem. 17: 606-613. https://doi.org/10.1016/j.bmc.2008.11.066 PMid:19101157

  • Mazet I, Vey A. 1995. Hirsutellin A, a toxic protein produced in vitro by Hirsutella thompsonii. Microbiology 141(6): 1343-1348. https://doi.org/10.1099/13500872-141-6-1343 PMid:7670635

  • Mil-Homens D, Bernardes N, Fialho AM. 2012. The antibacterial properties of docosahexaenoic omega-3 fatty acid against the cystic fibrosis multiresistant pathogen Burkholderia cenocepacia. FEMS Microbiol Lett. 328(1): 61-69. https://doi.org/10.1111/j.1574-6968.2011.02476.x PMid:22150831

  • Oh TJ, Hyun SH, Lee SG, Chun YJ, Sung GH. 2014. NMR and GC-MS based metabolic profiling and free-radical scavenging activities of Cordyceps pruinosa mycelia cultivated under different media and light conditions. PLoS ONE 9(3): e90823. https://doi.org/10.1371/journal.pone.0090823 PMid:24608751 PMCid:PMC3946585

  • Oller-López JL, Iranzo M, Mormeneo S, Oliver E, Cuerva JM, Oltra JE. 2005. Bassianolone: an antimicrobial precursor of cephalosporolides E and F from the entomoparasitic fungus Beauveria bassiana. Org Biomol Chem. 3(7): 1172-1173. https://doi.org/10.1039/B417534D PMid:15785802

  • Ortiz-Urquiza A, Fan Y, Garrett T, Keyhani NO. 2016. Growth substrates and caleosin-mediated functions affect conidial virulence in the insect pathogenic fungus Beauveria bassiana. Microbiology 162(11): 1913-1921. https://doi.org/10.1099/mic.0.000375 https://doi.org/10.1099/mic.0.000375 PMid:27655425

  • Paulraj MG, Reegan AD, Ignacimuthu S. 2011. Toxicity of Benzaldehyde and Propionic Acid against Immatureand Adult Stages of Aedes aegypti (Linn.) and Culex quinquefasciatus (Say) (Diptera: Culicidae). J Entomol. 8: 539-547. https://doi.org/10.3923/je.2011.539.547

  • Ragavendran C, Dubey NK, Natarajan D. 2017. Beauveria bassiana (Clavicipitaceae): a potent fungal agent for controlling mosquito vectors of Anopheles stephensi, Culex quinquefasciatus and Aedes aegypti (Diptera: Culicidae). RSC Advances. 7(7): 3838-3851. https://doi.org/10.1039/C6RA25859J

  • Ramadan Z, Jacobs D, Grigorov M, Kochhar S. 2006. Metabolic profiling using principal component analysis, discriminant partial least squares, and genetic algorithms. Talanta 68: 1683-1691. https://doi.org/10.1016/j.talanta.2005.08.042 PMid:18970515

  • Rohrlich C, Merle I, MzeHassani I, Verger M, Zuin M, Besse S. 2018. Variation in physiological host range in three strains of two species of the entomopathogenic fungus Beauveria. PLoS ONE 13(7): e0199199. https://doi.org/10.1371/journal.pone.0199199 PMid:29975710 PMCid:PMC6033404

  • Sayed AM, Behle RW, Tiilikkala K, Vaughn SF. 2018. Insecticidal activity of bio-oils and biochar as pyrolysis products and their combination with microbial agents against Agrotis ipsilon (Lepidoptera: Noctuidae). Pestic Phytomed. 33(1): 39-52. https://doi.org/10.2298/PIF1801039S

  • Smedsgaard J. 1997. Micro-scale extraction procedure for standardized screening of fungal metabolite production in cultures. J Chromatogr A 760(2): 264-270. https://doi.org/10.1016/s0021-9673(96)00803-5

  • Strasser H, Abendstein D, Stuppner H, Butt TM. 2000. Monitoring the distribution of secondary metabolites produced by the entomogenous fungus Beauveria brongniartii with particular reference to oosporein. Mycol Res. 104: 1227-1233. https://doi.org/10.1017/S0953756200002963

  • Strasser H, Vey A, Butt TM. 2000. Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species? Biocontrol Sci Technol. 10: 717-735. https://doi.org/10.1080/09583150020011690

  • Talaei-Hassanloui R, Kharazi-Pakdel A, Goettel M, Mozaffari J. 2006. Variation in virulence of Beauveria bassiana isolates and its relatedness to some morphological characteristics. Biocontrol Sci Technol. 16(5): 525534. https://doi.org/10.1080/09583150500532758

  • Valero-Jiménez CA, Debets AJ, van Kan JA, Schoustra SE, Takken W, Zwaan BJ. 2014. Natural variation in virulence of the entomopathogenic fungus Beauveria bassiana against malaria mosquitoes. Malar J. 13(1):1-8. https://doi.org/10.1186/1475-2875-13-479 PMid:25480526 PMCid:PMC4364330

  • Vey A, Hoagland R, Butt TM. 2001. Toxic metabolites of fungal biocontrol agents, pp. 311-345. In: Butt TM, Jackson CW. and Magan N. (Eds.). Fungi as Biocontrol Agents: Potential, Progress and Problems. CAB International, Wallingford, UK. https://doi.org/10.1079/9780851993560.0311

  • Vivekanandhan P, Kavitha T, Karthi S, Senthil-Nathan S, Shivakumar M. 2018. Toxicity of Beauveria bassiana-28 mycelial extracts on larvae of Culex quinquefasciatus mosquito (Diptera: Culicidae). Int J Environ Res Public Health 15(3): 440. https://doi.org/10.3390/ijerph15030440 PMid:29510502 PMCid:PMC5876985

  • Wakil W, Yasin M, Shapiro-Ilan D. 2017. Effects of single and combined applications of entomopathogenic fungi and nematodes against Rhynchophorus ferrugineus (Olivier). Sci Rep. 7(1): 5971. https://doi.org/10.1038/s41598-017-05615-3 PMid:28729649 PMCid:PMC5519636

  • Wahlman M, Davidson BS. 1993. New destruxins from the entomopathogenic fungus Metarhizium anisopliae. J Nat Prod. 56(4): 643-647. https://doi.org/10.1021/np9601216

  • Wang CS, Skrobek A, Butt TM. 2004. Investigations on the destruxin production of the entomopathogenic fungus Metarhizium anisopliae in liquid and solid media. J Invertebr Pathol. 85: 168-174. https://doi.org/10.1016/j.jip.2004.02.008 PMid:15109899

  • Woappi Y, Gabani P, Singh A, Singh O.V. 2016. Antibiotrophs: the complexity of antibiotic-subsisting and antibioticresistant microorganisms. Crit Rev Microbial. 42(1): 17-30. https://doi.org/10.3109/1040841X.2013.875982 PMid:24495094

  • Xu Y, Orozco R, Wijeratne EK, Espinosa-Artiles P, Gunatilaka AL, Stock SP, Molnár I. 2009. Biosynthesis of the cyclooligomer depsipeptide bassianolide, an insecticidal virulence factor of Beauveria bassiana. Fungal Genet Biol. 46(5): 353-364. https://doi.org/10.1016/j.fgb.2009.03.001 PMid:19285149

  • Xu Y, Orozco R, Wijeratne EMK, Gunatilaka AAL, Stock SP, Molnár I. 2008. Biosynthesis of the cyclooligomer depsipeptide beauvericin, a virulence factor of the entomopathogenic fungus Beauveria bassiana. Chem Biol. 15: 898-907. https://doi.org/10.1016/j.chembiol.2008.07.011 PMid:18804027

  • Zhang S, Widemann E, Bernard G, Lesot A, Pinot F, Pedrini N, Keyhani NO. 2012. CYP52X1, representing new cytochrome P450 subfamily, displays fatty acid hydroxylase activity and contributes to virulence and growth on insect cuticular substrates in entomopathogenic fungus Beauveria bassiana. J Biol Chem. 287(16): 13477-13486. https://doi.org/10.1074/jbc.M111.338947 aPMid:22393051 PMCid:PMC3339963


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  • Metabolome heterogeneity in the isolates of entomopathogenic fungus, Beauveria bassiana (Balsamo) Vuillemin

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Authors

P. R. Nithya
Department of Agricultural Entomology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India
S. Manimegalai
Department of Agricultural Entomology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India
S. Nakkeeran
Department of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India
S. Mohankumar
Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India
S. Jayarajan Nelson
Department of Agricultural Entomology, Tamil Nadu Agricultural University, Coimbatore – 641003, Tamil Nadu, India

Abstract


Entomopathogenic fungi are known to produce a multitude of low molecular weight secondary metabolites involved in different biological processes including fungal development, intercellular communication and interaction with other organisms in complex niches. In the present investigation, heterogeneity in metabolome profile of three isolates of Beauveria bassiana viz., MH590235 (TM), MK918495 (BR) and KX263275 (BbI8) were analyzed through GC-MS. Distinct differences in metabolite profile of the isolates were observed. A total of 63 metabolites were detected from all the isolates combined. Metabolites, 5-Oxotetrahydrofuran-2-carboxylic acid and undecane were found to be specific to BR isolate. Macrocyclic gamma lactones were detected in culture filtrates of BR and BbI8, oleic acid and hexadecanoic acid in TM and BR. An insecticidal compound, levoglucos an was detected in all the fungal isolates. Among the isolates, TM revealed higher variability in the metabolite production through PCA analysis. The metabolome of TM isolate contained compounds having several biological functions, viz., insecticidal and antimicrobial activity, lipid and fatty acid metabolisms and virulence enhancing factors.


Keywords


Beauveria bassiana, Biological Functions, GC-MS, Metabolome Heterogeneity, PCA Analysis.

References





DOI: https://doi.org/10.18311/jbc%2F2019%2F24302