Volatile Organic Compounds (VOC) Produced by Paraconiothyrium archidendri F10 as Biofungicidal Materials for Ganoderma boninense

Document Type : Original Research

Authors
Research Center for Applied Microbiology, National Research and Innovation Agency, Jl. Raya Jakarta-Bogor Km. 46, Cibinong, Bogor, West Java 16911, Indonesia.
Abstract
In this study, a soil fungus isolated from a healthy, disease-free oil palm plantation was evaluated for its inhibitory activity in vitro, with the aim of assessing its effectiveness as a bio-inoculant. The soil fungus was sequenced for the ITS-rDNA region, and its similarity was analyzed through bioinformatics using BLASTn searches and phylogenetic tree construction. Volatile Organic Compounds (VOCs) were produced through batch fermentation on Potato Dextrose Agar (PDA). The inhibitory activity against the radial growth of G. boninense was evaluated using the vapor assay method. The VOC profile and other metabolites were analyzed using GC-MS. The inhibitory mechanism between VOCs and target proteins was studied through in silico analysis. VOCs produced by P. archidendri F10 were found to inhibit G. boninense mycelium growth by up to 55.8% in four days, with the mycelium exhibiting wavy, non-smooth, and wrinkled morphology, abnormal branching, fused, defective hyphae, and lysis through microscopy imaging. The molecular docking analysis revealed that 7,9-ditert-butyl-1-oxaspiro[4.5]deca-6,9-diene-2,8-dione had the strongest binding affinity at -8.5 kcal mol-1, forming one hydrogen bond with Tyr646 at a distance of 2.98 Å. Another notable ligand was 2-O-(6-ethyloctan-3-yl) 1-O-hexyl oxalate, with a binding affinity of -5.6 kcal mol-1 and one hydrogen bond with His698 at 3.05 Å. The remaining ligands did not form hydrogen bonds. Thus, P. archidendri F10 has potential as a biofungicide for controlling G. boninense in the future.

Keywords

Subjects


1.       Bismarck, D., Dusold, A., Heusinger, A. and Muller, E. 2019. Antifungal in vitro Activity of Essential Oils against Clinical Isolates of Malassezia pachydermatis from Canine Ears: A Report from a Practice Laboratory. Complement. Med. Res., 27: 143-154.
2.       Don, S. M. Y., Schmidtke, L. M., Gambetta, J. M. and Steel, C. C. 2021. Volatile Organic Compounds Produced by Aureobasidium pullulans Induce Electrolyte Loss and Oxidative Stress in Botrytis cinerea and Alternaria alternata. Res. Microbiol., 172: 103788.
3.       Dover, L. G., Alderwick, L. J., Brown, A. K., Futterer, K. and Besra, G. S. 2007. Regulation of Cell Wall Synthesis and Growth. Curr. Mol. Med.7: 247-276.
4.       Emanuel, R. V., César Arturo, P. U., Lourdes Iveth, M. R., Homero, R. D. L. C. and Nahuam, C. A. M. 2020. In Vitro Growth of Colletotrichum gloeosporioides is Affected by Butyl Acetate, A Compound Produced during The Co-Culture of Trichoderma sp. and Bacillus subtilis3 Biotech10: 1-14.
5.       Fang, W., Yan, D., Wang, X., Huang, B., Wang, X., Liu, J., Liu, X., Li, Y., Ouyang, C., Wang, Q. and Cao, A. 2018. Responses of Nitrogen-Cycling Microorganisms to Dazomet Fumigation. Front. Microbiol., 9: 2529.
6.       Farbo, M. G., Urgeghe, P. P., Fiori, S., Marcello, A., Oggiano, S., Balmas, V., Hassan, Z. U., Jaoua, S. and Migheli, Q. 2018. Effect of Yeast Volatile Organic Compounds on Ochratoxin A-Producing Aspergillus carbonarius and A. ochraceus. Int. J. Food Microbiol., 284: 1-10.
7.       Filonow, A. B. 2002. Mycoactive Acetate Esters from Apple Fruit Stimulate Adhesion and Germination of Conidia of the Gray Mold Fungus. J. Agric. Food Chem.50: 3137-3142.
8.       Gow, N. A. R., Latge, J. P. and Munro, C. A. 2017. The Fungal Cell Wall: Structure, Biosynthesis, and Function. Microbiol. Spectr., 5: 10-1128.
9.       Han, M., Liu, T., Cai, X., Chen, K., Liu, C., Brian, K., Xue, Y. and Gu, Y. 2012. A New Endophytic Paraconiothyrium brasiliens LT161 Shows Potential in Producing Antifungal Metabolites against Phytopathogens. Afr. J. Microbiol. Res., 6: 7572-7578.
10.    Hartanto, A., Munir, E., Basyuni, M., Saleh, M. N., Hastuti, L. D. S., Yurnaliza, Y., Nurtjahja, K. and Lutfia, A. 2023. Antifungal Activity of Volatile Organic Compounds (VOC) by an Endophytic Fungus, Lasiodiplodia avicenniae P2P4 from Avicennia alba against Fusarium oxysporum. Rasayan J. Chem., 16: 182-187.
11.    Ibe, C. and Munro, C. A. 2021. Fungal Cell Wall: An Underexploited Target for Antifungal Therapies. PLoS Pathog., 17: e1009470.
12.    Isha, A., Yusof, N. A., Shaari, K., Osman, R., Abdullah, S. N. A. and Wong, M. Y. 2020. Metabolites Identification of Oil Palm Roots Infected with Ganoderma boninense using GC–MS-based Metabolomics. Arab. J. Chem., 13: 6191-6200.
13.    Islamiati, E. D., Widada, J., Wahyuningsih, T. D. and Widianto, D. 2022. Volatile Organic Compounds of Streptomyces sp. GMR22 Inhibit Growth of Two Plant Pathogenic Fungi. Agric. Nat. Res., 56: 899-908.
14.    Kong, W. L., Ni, H., Wang, W. Y. and Wu, X. Q. 2022. Antifungal Effects of Volatile Organic Compounds Produced by Trichoderma koningiopsis T2 against Verticillium dahliae. Front. Microbiol., 13: 1013468.
15.    Jayakar, V., Lokapur, V. and Shantaram, M. 2020. Identification of the Volatile Bioactive Compounds by GC-MS Analysis from the Leaf Extracts of Garcinia cambogia and Garcinia indica. Med. Plant., 12: 580-590.
16.    Latz, M. A. C., Jensen, B., Collinge, D. B. and Jørgensen, H. J. L. 2018. Endophytic Fungi as Biocontrol Agents: Elucidating Mechanisms in Disease Suppression. Plant Ecol. Divers., 11: 555-567.
17.    Maluin, F. N., Hussein, M. Z. and Idris, A. S. 2020. An Overview of the Oil Palm Industry: Challenges and Some Emerging Opportunities for Nanotechnology Development. Agronomy, 10: 356.
18.    Pachaiappan, R., Nagasathiya, K., Singh, P. K., Gopalakrishnan, A.V., Velusamy, P., Ramasamy, K., Velmurugan, D., Kandasamy, R., Ramasamy, P. and Gopinath, S. C. B. 2022. Phytochemical Profile of Black Cumin (Nigella sativa L.) Seed Oil: Identification of Bioactive Anti-Pathogenic Compounds for Traditional Siddha Formulation. Biomass Convers. Biorefin., 13: 14683-14695.
19.    Patel, D., Shittu, T. A., Baroncelli, R., Muthumeenakshi, S., Osborne, T. H., Janganan, T. K. and Sreenivasaprasad, S. 2021. Genome Sequence of the Biocontrol Agent Coniothyrium minitans Conio (IMI 134523). Mol. Plant Microbe Interact., 34: 222-225.
20.    Paterson, R. R. M. 2019. Ganoderma boninense Disease of Oil Palm to Significantly Reduce Production After 2050 in Sumatra if Projected Climate Change Occurs. Microorganisms, 7: 24.
21.    Pimenta, R. S., da Silva, J. F. M., Buyer, J. S. and Janisiewicz, W. J. 2012. Endophytic Fungi from Plums (Prunus domestica) and Their Antifungal Activity against Monilinia fructicola. J. Food Prot., 75: 1883-1889.
22.    Rao, Y., Zeng, L., Jiang, H., Mei, L. and Wang, Y. 2022. Trichoderma atroviride LZ42 Releases Volatile Organic Compounds Promoting Plant Growth and Suppressing Fusarium Wilt Disease in Tomato Seedlings. BMC Microbiol., 22: 88.
23.    Rego, A., Duarte, A. M., Azevedo, F., Sousa, M. J., Corte-Real, M. and Chaves, S. R. 2014. Cell Wall Dynamics Modulate Acetic Acid-Induced Apoptotic Cell Death of Saccharomyces cerevisiae. Microb. Cell, 1: 303-314.
24.    Rhetso, T., Seshadri, R. M., Ramnath, S. and Venkataramegowda, S. 2021. GC-MS based Metabolite Profiling and Antioxidant Activity of Solvent Extracts of Allium chinense G Don Leaves. Not. Sci. Biol., 13: 10791.
25.    Rozlianah, F. S., Jualang, A. G. and Chong, K. P. 2015. Fatty Acids and Phenols Involved in Resistance of Oil Palm to Ganoderma boninense. Adv. Environ. Biol., 9: 11-16.
26.    Ruiz-Moyano, S., Hernandez, A., Galvan, A. I., Cordoba, M. G., Casquete, R., Serradilla, M. J. and Martin, A. 2020. Selection and Application of Antifungal VOCs-Producing Yeasts as Biocontrol Agents of Grey Mould in Fruits. Food Microbiol., 92: 103556.
27.    Saxena, S. and Strobel, G. A. 2021. Marvellous Muscodor spp.: Update on Their Biology and Applications. Microb. Ecol., 82: 5-20.
28.    Sharma, M., Saini, S., Soniya and Agrawal, R. D. 2019. Isolation and Identification of Phytosterols from Anogeissus pendula (Edgew) and Their Antimicrobial Potency. J. Pharmacogn. Phytochem., 8: 1665-1670.
29.    Spadaro, D. and Droby, S. 2016. Development of Biocontrol Products for Postharvest Diseases of Fruit: The Importance of Elucidating the Mechanisms of Action of Yeast Antagonists. Trend. Food Sci. Technol., 47: 39-49.
30.    Tabassum, S., Ahmad, S., Khan, K. R., Ali, B., Usman, F., Jabeen, Q., Sajid-ur-Rehman, M., Ahmed, M., Zubair, H. M., Alkazmi, L., Batiha, G. E. S., Qamar-uz-Zaman and Basit, A. 2023. Chemical Profiling and Evaluation of Toxicological, Antioxidant, Anti-Inflammatory, Anti-Nociceptive and Tyrosinase Inhibitory Potential of Portulacaria afra using In-Vitro, In-Vivo and In-Silico Studies. Arab. J. Chem., 16: 104784.
31.    Tatipamula, V. B., Killari, K. N., Prasad, K., Rao, G. S. N. K., Talluri, M. R., Vantaku, S., Bilakanti, D. and Srilakshmi, N. 2019. Cytotoxicity Studies of the Chemical Constituents from Marine Algae Chara baltica. Ind. J. Pharm. Sci., 81: 815-823.
32.    Tennakoon, D. S., Thambugala, K. M., de Silva, N. I., Suwannarach, N. and Lumyong, S. 2022. A Taxonomic Assessment of Novel and Remarkable Fungal Species in Didymosphaeriaceae (Pleosporales, Dothideomycetes) from Plant Litter. Front. Microbiol., 13: 1016285.
33.    Tilocca, B., Cao, A. and Migheli, Q. 2020. Scent of a Killer: Microbial Volatilome and Its Role in the Biological Control of Plant Pathogens. Front. Microbiol., 11: 41.
34.    Verkley, G. J. M., Dukik, K., Renfurm, R., Göker, M. and Stielow, J. B. 2014. Novel Genera and Species of Coniothyrium-like Fungi in Montagnulaceae (Ascomycota). Persoonia, 32: 25-51.
35.    Wanasinghe, D. N. and Mortimer, P. E. 2022. Taxonomic and Phylogenetic Insights into Novel Ascomycota from Forest Woody Litter. Biology, 11: 889.
36.    Widada, J., Damayanti, E., Alhakim, M. R., Yuwono, T. and Mustofa, M. 2021. Two Strains of Airborne Nocardiopsis alba Producing Different Volatile Organic Compounds (VOCs) as Biofungicide for Ganoderma boninense. FEMS Microbiol. Lett., 368(20): 1-10
37.    Yang, Y., Chen, Y., Cai, J., Liu, X. and Huang, G. 2021. Antifungal Activity of Volatile Compounds Generated by Endophytic Fungi Sarocladium brachiariae HND5 against Fusarium oxysporum f. sp. cubense. PLoS One, 16: e0260747.
38.    Yurnaliza, Y., Jamilah, I., Hartanto, A. and Lutfia, A. 2021. Screening of Endophytic Fungi from Oil Palm (Elaeis guineensis) in Producing Exopolysaccharides. Biodiversitas, 22: 1467-1473.
39.    Zhang, Y., Crous, P. W., Schoch, C. I. and Hyde, K. D. 2012. Pleosporales. Fungal Divers., 52: 1-225.
40.   Zhang, J., Jiang, H., Du, Y., Keyhani, N. O., Xia, Y., and Jin, K. 2019. Members of Chitin Synthase Family in Metarhizium acridum Differentially Affect Fungal Growth, Stress Tolerances, Cell Wall Integrity and Virulence. PLoS Pathog.15: e1007964.