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Production of Volatile Compounds by a Variety of Fungi in Artificially Inoculated and Naturally Infected Aquilaria malaccensis

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Abstract

Aquilaria malaccensis, the resinous agarwood, is highly valued in the perfumery and medicinal industry. The formation of fragrant agarwood resin inconsistently by various fungi is still not clearly understood. The current study investigated the agarwood quality and fungal diversity in artificially inoculated and naturally infected A. malaccensis. The chemical analysis of volatile compounds of agarwood was performed using the Solid Phase Micro Extraction (SPME) method, and the identification of fungi was made through a morphological observation using a light microscope. Gas chromatography analysis revealed the presence of essential compounds related to high-quality agarwood, such as 4-phenyl-2-butanone, β-selinene, α-bulnesene, and agarospirol in both artificially inoculated and naturally infected agarwood but with some differences in the abundance. Further studies on the fungi associated with agarwood volatile compounds formation showed a total of ten fungal group isolates, which were identified based on morphological and molecular studies. The study revealed that agarwood from both artificial and natural sources were naturally infected with Fusarium, Botryosphaeria, Aspergillus, Schizophyllum, Phanerochaete, Lasiodiplodia, Polyporales, and Ceriporia species. This study has offered a potential opportunity to research further the promising development of fungal strains for artificial inducement of high-quality agarwood formation from A. malaccensis trees.

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References

  1. Rasool S., Mohamed R. (2016) Understanding Agarwood Formation and Its Challenges. In: Mohamed R (eds) Agarwood Tropical Forestry Springer, Singapore Doi: https://doi.org/10.1007/978-981-10-0833-7_3

  2. Chhipa H, Kaushik N (2017) Fungal and bacterial diversity isolated from Aquilaria malaccensis tree and soil, induces agarospirol formation within 3 months after artificial infection. Front Microbiol 8:1286. https://doi.org/10.3389/fmicb.2017.01286

    Article  PubMed  PubMed Central  Google Scholar 

  3. Faizal A, Esyanti RR, Aulianisa EN et al (2017) Formation of agarwood from Aquilaria malaccensis in response to inoculation of local strains of Fusarium solani. Trees 31:189–197. https://doi.org/10.1007/s00468-016-1471-9

    Article  Google Scholar 

  4. Turjaman M., Hidayat A., Santoso E. (2016) Development of Agarwood Induction Technology Using Endophytic Fungi. In: Mohamed R. (eds) Agarwood. Tropical Forestry. Springer, Singapore https://doi.org/10.1007/978-981-10-0833-7_4

  5. Barden A, Anak NA, Mulliken T, Song M. Heart of the matter: agarwood use and trade and CITES implementation for Aquilaria malaccensis. TRAFFIC International, Cambridge, UK. 2000 Aug.

  6. Bhuyar P, Rahim MH, Sundararaju S, Maniam GP, Govindan N (2020) Antioxidant and antibacterial activity of red seaweed Kappaphycus alvarezii against pathogenic bacteria. Global J Environ Sci Manag 6(1):47–58. https://doi.org/10.22034/GJESM.2020.01.04

    Article  CAS  Google Scholar 

  7. Jayachandran KS, Sekar I, Parthiban KT, Amirtham D, Suresh KK (2015) Analysis of different grades of agarwood (Aquilaria malaccensis Lamk.) oil through GC-MS. Indian Journal of Natural Products and Resources (IJNPR) 5(1):44–47

    Google Scholar 

  8. Chua LS (2008) Agarwood (Aquilaria malaccensis) in Malaysia. Forest Research Institute Malaysia

  9. Bhuiyan MN, Begum J, Bhuiyan MN (2009) Analysis of essential oil of eaglewood tree (Aquilaria agallocha Roxb) by gas chromatography mass spectrometry. Bangladesh J Pharmacol 4(1):24–28. https://doi.org/10.3329/bjp.v4i1.85

    Article  Google Scholar 

  10. Premalatha K, Kalra AJ (2013) Molecular phylogenetic identification of endophytic fungi isolated from resinous and healthy wood of Aquilaria malaccensis, a red listed and highly exploited medicinal tree. Fungal Ecol 6(3):205–211. https://doi.org/10.1016/j.funeco.2013.01.005

    Article  Google Scholar 

  11. Mohamed R, Jong PL, Zali MS (2010) Fungal diversity in wounded stems of Aquilaria malaccensis. Fungal Diversity 43:67–74. https://doi.org/10.1007/s13225-010-0039-z

    Article  Google Scholar 

  12. Monggoot S, Kulsing C, Wong YF et al (2018) Incubation of aquilaria subintegra with microbial culture supernatants enhances production of volatile compounds and improves quality of agarwood oil. Indian J Microbiol 58:201–207. https://doi.org/10.1007/s12088-018-0717-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bhuyar P, Rahim MHA, Maniam GP et al (2020) Exploration of bioactive compounds and antibacterial activity of marine blue-green microalgae (Oscillatoria sp) isolated from coastal region of west Malaysia. SN Appl. Sci. 2:1906. https://doi.org/10.1007/s42452-020-03698-8

    Article  CAS  Google Scholar 

  14. Ferreira JH, Matthee FN, Thomas AC (1991) Biological control of Eutypa lata on grapevine by an antagonistic strain of Bacillus subtilis. Phytopathology 81(3):283–287

    Article  Google Scholar 

  15. Ramli AN, Hamid HA, Zulkifli FH, Zamri N, Bhuyar P, Manas NH (2021) Physicochemical properties and tenderness analysis of bovine meat using proteolytic enzymes extracted from pineapple (Ananas comosus) and jackfruit (Artocarpus heterophyllus) by-products. J Food Process Preserv 45(11):e15939. https://doi.org/10.1111/jfpp.15939

    Article  CAS  Google Scholar 

  16. Ramli AN, Sukri NA, Azelee NI, Bhuyar P (2021) Exploration of antibacterial and antioxidative activity of seed/peel extracts of Southeast Asian fruit Durian (Durio zibethinus) for effective shelf-life enhancement of preserved meat. J Food Process Preserv 45(9):e15662. https://doi.org/10.1111/jfpp.15662

    Article  CAS  Google Scholar 

  17. Chehri K, Salleh B, Zakaria L (2015) Morphological and phylogenetic analysis of Fusarium solani species complex in Malaysia. Microb Ecol 69(3):457–471. https://doi.org/10.1007/s00248-014-0494-2

    Article  PubMed  Google Scholar 

  18. Ploetz RC (2015) Fusarium wilt of banana. Phytopathology 105:1512–1521

    Article  PubMed  Google Scholar 

  19. Norhayati M, Erneeza MH, Kamaruzaman S (2016) Morphological, pathogenic and molecular characterization of Lasiodiplodia theobromae A causal pathogen of black rot disease on kenaf seeds in Malaysia. Int J Agricult Biol 18(1):80–85. https://doi.org/10.17957/IJAB/15.0065

    Article  CAS  Google Scholar 

  20. Zhang Y, Liu HX, Li WS, Tao MH, Pan QL, Sun ZH, Ye W, Li HH, Zhang WM (2017) 2-(2-phenylethyl) chromones from endophytic fungal strain Botryosphaeria rhodina A13 from Aquilaria sinensis. Chinese Herbal Medicines 9(1):58–62. https://doi.org/10.1016/S1674-6384(17)60076-5

    Article  Google Scholar 

  21. Mishra A, Gond SK, Kumar A, Sharma VK, Verma SK, Kharwar RN, Sieber TN (2012) Season and tissue type affect fungal endophyte communities of the Indian medicinal plant Tinospora cordifolia more strongly than geographic location. Microb Ecol 64(2):388–398. https://doi.org/10.1007/s00248-012-0029-7

    Article  PubMed  Google Scholar 

  22. Mohamed R, Jong PL, Nurul Irdayu I (2014) Succession patterns of fungi associated to wound-induced agarwood in wild Aquilaria malaccensis revealed from quantitative PCR assay. World J Microbiol Biotechnol 30:2427–2436. https://doi.org/10.1007/s11274-014-1668-2

    Article  CAS  PubMed  Google Scholar 

  23. Sales AC, Yoshizawa T (2005) Updated profile of aflatoxin and Aspergillus section Flavi contamination in rice and its byproducts from the Philippines. Food Addit Contam 22(5):429–436. https://doi.org/10.1080/02652030500058387

    Article  CAS  PubMed  Google Scholar 

  24. Singh PK, Kathuria S, Agarwal K, Gaur SN, Meis JF, Chowdhary A (2013) Clinical significance and molecular characterization of nonsporulating molds isolated from the respiratory tracts of bronchopulmonary mycosis patients with special reference to basidiomycetes. J Clin Microbiol 51(10):3331–3337. https://doi.org/10.1128/JCM.01486-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Teoh Y, Mashitah MD, Salmiah U (2017) Production of biomass by Schizophyllum commune and its antifungal activity towards rubberwood-degrading fungi. Sains Malaysiana 46(1):123–128

    Article  CAS  Google Scholar 

  26. Zulkarnain A, Bahrin EK, Ramli N et al (2018) Alkaline hydrolysate of oil palm empty fruit bunch as potential substrate for biovanillin production via two-step bioconversion. Waste Biomass Valor 9:13–23. https://doi.org/10.1007/s12649-016-9745-4

    Article  CAS  Google Scholar 

  27. Sultan S, Sun L, Blunt JW, Cole AL, Munro MH, Ramasamy K, Weber JF (2014) Evolving trends in the dereplication of natural product extracts. 3: further lasiodiplodins from Lasiodiplodia theobromae, an endophyte from Mapania kurzii. Tetrahedron Lett 55(2):453–455. https://doi.org/10.1016/j.tetlet.2013.11.060

    Article  CAS  Google Scholar 

  28. El-Fadaly HM, El-Kadi SM, Hamad MN, Habib AA (2015) Isolation and identification of egyptian ras cheese (Romy) contaminating fungi during ripening period. J Microbiol Res 5:1–10

    Google Scholar 

  29. Krull R, Wucherpfennig T, Esfandabadi ME, Walisko R, Melzer G, Hempel DC, Kampen I, Kwade A, Wittmann C (2013) Characterization and control of fungal morphology for improved production performance in biotechnology. J Biotechnol 163(2):112–123. https://doi.org/10.1016/j.jbiotec.2012.06.024

    Article  CAS  PubMed  Google Scholar 

  30. Nasution F, Theanhom AA, Bhuyar P, Chumpookam J (2021) Genetic diversity evaluation in wild Muntingia calabura L. based on Random Amplified Polymorphic DNA (RAPD) markers. Gene Reports 25:101335. https://doi.org/10.1016/j.genrep.2021.101335

    Article  Google Scholar 

  31. Raja HA, Miller AN, Pearce CJ, Oberlies NH (2017) Fungal identification using molecular tools: a primer for the natural products research community. J Nat Prod 80(3):756–770. https://doi.org/10.1021/acs.jnatprod.6b01085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W (2012) Fungal Barcoding Consortium Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109(16):6241–6246. https://doi.org/10.1073/pnas.1117018109

    Article  PubMed  PubMed Central  Google Scholar 

  33. Min XJ, Hickey DA (2007) Assessing the effect of varying sequence length on DNA barcoding of fungi. Mol Ecol Notes 7(3):365–373. https://doi.org/10.1111/j.1471-8286.2007.01698.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ismail N, Ali NA, Jamil M, Rahiman MH, Tajuddin SN, Taib MN (2014) A review study of agarwood oil and its quality analysis. Jurnal Teknologi. https://doi.org/10.11113/jt.v68.2419

    Article  Google Scholar 

  35. Tajuddin SN, Yusoff MM (2010) Chemical composition of volatile oils of Aquilaria malaccensis (Thymelaeaceae) from Malaysia. Natural Product Commun 5(12):1934. https://doi.org/10.1177/1934578X1000501229

    Article  Google Scholar 

  36. Zhang XL, Liu YY, Wei JH, Yang Y, Zhang Z, Huang JQ, Chen HQ, Liu YJ (2012) Production of high-quality agarwood in Aquilaria sinensis trees via whole-tree agarwood-induction technology. Chin Chem Lett 23(6):727–730. https://doi.org/10.1016/j.cclet.2012.04.019

    Article  CAS  Google Scholar 

  37. Liu Y, Chen H, Yang Y, Zhang Z, Wei J, Meng H, Chen W, Feng J, Gan B, Chen X, Gao Z (2013) Whole-tree agarwood-inducing technique: an efficient novel technique for producing high-quality agarwood in cultivated Aquilaria sinensis trees. Molecules 18(3):3086–3106. https://doi.org/10.3390/molecules18033086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ponzio C, Gols R, Pieterse CM, Dicke M (2013) Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Funct Ecol 27(3):587–598. https://doi.org/10.1111/1365-2435.12035

    Article  Google Scholar 

  39. Ishihara M, Tsuneya T, Uneyama K (1993) Fragrant sesquiterpenes from agarwood. Phytochemistry 33(5):1147–1155. https://doi.org/10.1016/0031-9422(93)85039-T

    Article  CAS  Google Scholar 

  40. Wetwitayaklung P, Thavanapong N, Charoenteeraboon J (2009) Chemical constituents and antimicrobial activity of essential oil and extracts of heartwood of Aquilaria crassna obtained from water distillation and supercritical fluid carbon dioxide extraction. Science, Engineering and Health Studies. https://doi.org/10.14456/sustj.2009.3

    Article  Google Scholar 

  41. Naef R (2011) The volatile and semi-volatile constituents of agarwood, the infected heartwood of Aquilaria species: a review. Flavour Fragr J 26(2):73–87. https://doi.org/10.1002/ffj.2034

    Article  CAS  Google Scholar 

  42. Ismail N, Rahiman MH, Taib MN, Ibrahim M, Zareen S, Tajuddin SN. Observation on SPME different headspace fiber coupled with GC-MS in extracting high quality agarwood chipwood. In2016 IEEE International Conference on Automatic Control and Intelligent Systems (I2CACIS) 2016 Oct 22 (pp. 214–218). IEEE. https://doi.org/10.1109/I2CACIS.2016.7885317

  43. Gratani L (2014) Plant phenotypic plasticity in response to environmental factors. Adv Botany 22:2014

    Google Scholar 

  44. Gouinguené SP, Turlings TC (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129(3):1296–1307. https://doi.org/10.1104/pp.001941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ramli ANM, Manap NWA, Bhuyar P et al (2020) Passion fruit (Passiflora edulis) peel powder extract and its application towards antibacterial and antioxidant activity on the preserved meat products. SN Appl Sci 2:1748. https://doi.org/10.1007/s42452-020-03550-z

    Article  CAS  Google Scholar 

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Acknowledgements

We acknowledged the Bio Aromatic Research Centre of Excellent and Faculty of Industrial Sciences & Technology, University Malaysia Pahang, to carry out this study. This project was funded by Universiti Malaysia Pahang (RDU182207-1).

Funding

This work was supported by Universiti Malaysia Pahang (Grant Number: RDU182207-1).

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Conceptualization: SY, ANMR; Methodology: SY, AWA; Formal analysis and investigation: SY, SNT; Writing—original draft preparation: SY, AWA; Writing—review and editing: SY, PB, HAH; Funding acquisition: ANMR; Resources: ANMR; Supervision: ANMR.

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Correspondence to Aizi Nor Mazila Ramli.

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I, Aizi Nor Mazila Ramli hereby declare that I participated in the study and in the development of the manuscript titled “Production of volatile compounds by various fungi in artificially inoculated and naturally infected Aquilaria malaccensis”. I have read the final version and give my consent for the article to be published in Current Microbiology.

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Ramli, A.N.M., Yusof, S., Bhuyar, P. et al. Production of Volatile Compounds by a Variety of Fungi in Artificially Inoculated and Naturally Infected Aquilaria malaccensis. Curr Microbiol 79, 151 (2022). https://doi.org/10.1007/s00284-022-02840-6

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