PERTANIKA JOURNAL OF SCIENCE AND TECHNOLOGY

Oil palm frond (OPF) is a palm oil plantation by-product commonly used in animal feeding in Malaysia. The large production, availability, and nutrient content make OPF the best candidate for utilization as animal feed. However, OPF contains high lignin bonds to cellulose and hemicellulose that further limit the digestibility of rumen microbes to produce volatile fatty acids as an energy source for ruminants. This study aims to identify and determine the enzyme activity (ligninolytic, cellulolytic, and hemicellulolytic) of enzymes extracted from filamentous fungi in the pre-treatment of OPF using the solid-state fermentation (SSF) technique. The enzyme extracted from SSF was determined by its enzyme activity (laccase, lignin peroxidase, manganese peroxidase, carboxymethylcellulose, avicelase, and xylanase). Eight fungi were successfully identified to produce enzymes determined in this experiment. Phanerina mellea showed the highest average ligninolytic enzyme activity with a value of 0.37 U/mL and an average cellulolytic + hemicellulolytic of 0.18 U/mL. In this experiment, P. mellea was the most desired fungi for the pre-treatment of OPF. The optimum ligninolytic enzyme production time of OPF pre-treatment is 10 days of SSF.

• Abdel-Hamid, A. M., Solbiati, J. O., & Cann, I. K. (2013). Insights into lignin degradation and its potential industrial applications. Advances in Applied Microbiology, 82, 1–28. https://doi.org/10.1016/B978-0-12-407679-2.00001-6

• Akpinar, M., & Urek, R. O. (2012). Production of ligninolytic enzymes by solid-state fermentation using Pleurotus eryngii. Preparative Biochemistry and Biotechnology, 42(6), 582–597. https://doi.org/10.1080/10826068.2012.673528

• Asgher, M., Bhatti, H. N., Ashraf, M., & Legge, R. L. (2008). Recent developments in biodegradation of industrial pollutants by white rot fungi and their enzyme system. Biodegradation, 19(6), 771-783. https://doi.org/10.1007/s10532-008-9185-3

• Azmi, M. A., Yusof, M. T., Zunita, Z., & Hassim, H. A. (2019). Enhancing the utilization of oil palm fronds as livestock feed using biological pre-treatment method. IOP Conference Series: Earth and Environmental Science, 230(1), Article 12077. https://doi.org/10.1088/1755-1315/230/1/012077

• Buayairaksa, M., Kanokmedhakul, S., Kanokmedhakul, K., Moosophon, P., Hahnvajanawong, C., & Soytong, K. (2011). Cytotoxic lasiodiplodin derivatives from the fungus Syncephalastrum racemosum. Archives of Pharmacal Research, 34(12), 2037–2041. https://doi.org/10.1007/s12272-011-1205-x

• Chanjula, P., Petcharat, V., & Cherdthong, A. (2017). Effects of fungal (Lentinussajor-caju) treated oil palm frond on performance and carcass characteristics in finishing goats. Asian-Australasian Journal of Animal Sciences, 30(6), Article 811. https://doi.org/10.5713/ajas.16.0704

• Chandran, B., & Nigam, P. (2001). Studies on the production of enzymes by white-rot fungi for the decolourisation of textile dyes. Enzyme and Microbial Technology, 29(8-9), 575–579. https://doi.org/10.1016/S0141-0229(01)00430-6

• Colombatto, D., Morgavi, D. P., Furtado, A. F., & Beauchemin, K. A. (2003). Screening of exogenous enzymes for ruminant diets: Relationship between biochemical characteristics and in vitro ruminal degradation. Journal of Animal Science, 81(10), 2628–2638. https://doi.org/10.2527/2003.81102628x

• Dinis, M. J., Bezerra, R. M. F., Nunes, F., Dias, A. A., Guedes, C. V, Ferreira, L. M. M., Cone, J. W., Marques, G. S. M., Barros, A. R. N., & Rodrigues, M. A. M. (2009). Bioresource Technology Modification of wheat straw lignin by solid state fermentation with white-rot fungi. Bioresource Technology, 100(20), 4829–4835. https://doi.org/10.1016/j.biortech.2009.04.036

• Dong, X. Q., Yang, J. S., Zhu, N., Wang, E. T., & Yuan, H. L. (2013). Sugarcane bagasse degradation and characterization of three white-rot fungi. Bioresource Technology, 131, 443–451. https://doi.org/10.1016/j.biortech.2012.12.182

• Falade, A. O., Nwodo, U. U., Iweriebor, B. C., Green, E., Mabinya, L. V., & Okoh, A. I. (2017). Lignin peroxidase functionalities and prospective applications. MicrobiologyOpen, 6(1), Article e00394. https://doi.org/10.1002/mbo3.394

• Galal, F. H., AbuElnasr, A., Abdallah, I., Zaki, O., & Seufi, A. M. (2017). Culex (Culex) pipiens mosquitoes carry and harbor pathogenic fungi during their developmental stages. Journal of Clinical Practice and Research, 39(1), 1-6. https://doi.org/10.5152/etd.2017.16067

• Gautam, A., Kumar, A., Bharti, A. K., & Dutt, D. (2018). Rice straw fermentation by Schizophyllum commune ARC-11 to produce high level of xylanase for its application in pre-bleaching. Journal of Genetic Engineering and Biotechnology, 16(2), 693–701. https://doi.org/10.1016/j.jgeb.2018.02.006

• Ghani, A. A. A., Rusli, N. D., Shahudin, M. S., Goh, Y. M., Zamri-Saad, M., Hafandi, A., & Hassim, H. A. (2017). Utilisation of oil palm fronds as ruminant feed and its effect on fatty acid metabolism. Pertanika Journal of Tropical Agricultural Science, 40(2), 215-224.

• Gupte, A., & Madamwar, D. (1997). Production of cellulolytic enzymes by coculturing of Aspergillus ellipticus and Aspergillus fumigatus grown on bagasse under solid state fermentation. Applied Biochemistry and Biotechnology, 62, 267–274. https://doi.org/10.1007/BF02788002

• Gupte, A., Gupte, S., & Patel, H. (2007). Ligninolytic enzyme production under solid-state fermentation by white rot fungi. Journal of Scientific and Industrial Research 66(08), 611–14.

• Hofrichter, M. (2002). Lignin conversion by manganese peroxidase (MnP). Enzyme and Microbial Technology, 30(4), 454–466. https://doi.org/10.1016/S0141-0229(01)00528-2

• Hu, H. L., Brink, J. Van Den, Gruben, B. S., Wösten, H. A. B., Gu, J., & Vries, R. P. De. (2011). International biodeterioration & biodegradation improved enzyme production by co-cultivation of Aspergillus niger and Aspergillus oryzae and with other fungi. International Biodeterioration & Biodegradation, 65(1), 248–252. https://doi.org/10.1016/j.ibiod.2010.11.008

• Islam, M., Dahlan, I., Rajion, M. A., & Jelan, Z. A. (2000). Productivity and nutritive values of different fractions of oil palm (Elaeis guineensis) frond. Asian-Australasian Journal of Animal Sciences, 13(8), 1113–1120. https://doi.org/10.5713/ajas.2000.1113

• Isroi, I., Millati, R., Niklasson, C., Cayanto, C., Taherzadeh, M. J., & Lundquist, K. (2011). Biological treatment of lignocelluloses with white-rot fungi and its applications. BioResources, 6(4), 5224–5259.

• Ji, L., Yang, J., Fan, H., Yang, Y., Li, B., Yu, X., Zhu, N., & Yuan, H. (2014). Synergy of crude enzyme cocktail from cold-adapted Cladosporium cladosporioides Ch2-2 with commercial xylanase achieving high sugars yield at low cost. Biotechnology for Biofuels, 7(1), Article 130. https://doi.org/10.1186/s13068-014-0130-x

• Khan, S. A., Hamayun, M., Yoon, H., Kim, H. Y., Suh, S. J., Hwang, S. K., Kim, J. M., Lee, I. J., Choo, Y. S., Yoon, U. H., Kong, W. S., Lee, B. M., & Kong, W. S. (2008). Plant growth promotion and Penicillium citrinum. BMC Microbiology, 8(1), Article 231. https://doi.org/10.1186/1471-2180-8-231

• Kumar, A., & Arora, P. K. (2022). Biotechnological applications of manganese peroxidases for sustainable management. Frontiers in Environmental Science, 10, Article 875157. https://doi.org/10.3389/fenvs.2022.875157

• Lima, A. C., Silva, D., Silva, V., Godoy, M., Cammarota, M., & Gutarra, M. (2021). β‐Mannanase production by Penicillium citrinum through solid‐state fermentation using açaí residual biomass (Euterpe oleracea). Journal of Chemical Technology & Biotechnology, 96(10), 2744–2754. https://doi.org/10.1002/jctb.6818

• Madhavi, V., & Lele, S. S. (2009). Laccase: Properties and applications. BioResources, 4(4), 1-24.

• Mäkelä, M. R., Hildén, K. S., & Kuuskeri, J. (2020). Fungal lignin-modifying peroxidases and H2O2-producing enzymes. In O. Zaragoza & A. Casdevall (Eds.) Encyclopedia of Mycology (pp. 247-259). Elsevier.

• Manavalan, T., Manavalan, A., & Heese, K. (2015). Characterization of lignocellulolytic enzymes from white-rot fungi. Current Microbiology, 70(4), 485–498. https://doi.org/10.1007/s00284-014-0743-0

• Mahmood, Z. A., & Azhar, I. (2017). Detection of aflatoxins and use of scanning electron microscope for the identification of fungal species in some commonly used spices. Asian Journal of Plant Science and Research, 7(5), 64–73.Miettinen, O., Spirin, V., Vlasák, J., Rivoire, B., Stenroos, S., & Hibbett, D. (2016). Polypores and genus concepts in Phanerochaetaceae (Polyporales, Basidiomycota). MycoKeys, 17, 1-46. https://doi.org/10.3897/mycokeys.17.10153

• Pant, D., & Adholeya, A. (2017). Enhanced production of ligninolytic enzymes and decolorization of molasses distillery wastewater by fungi under solid-state fermentation. Biodegradation, 18, 647–659. https://doi.org/10.1007/s10532-006-9097-z

• Ohm, R. A., Jong, J. F. De, Lugones, L. G., Aerts, A., Kothe, E., Stajich, J. E., de Vries, R. P., Record, E., Levasseur, A., Baker, S. E., Bartholomew, K. A., Coutinho, P. M., Erdmann, S., Fowler, T. J., Gathman, A. C., Lombard, V., Henrissat, B., Knabe, N., Kües, U., … & Wösten, H. A. B. (2010). Genome sequence of the model mushroom Schizophyllum commune. Nature Biotechnology, 28(9), 957-963. https://doi.org/10.1038/nbt.1643

• Parveez, G. K. A., Kamil, N. N., Zawawi, N. Z., Ong-Abdullah, M., Rasuddin, R., Loh, S. H., Selvadaray, K. R., Hoong, S. S., & Idris, Z. (2022). Oil palm economic performance in Malaysia and R&D progress in 2021. Journal of Oil Palm Research, 34(2), 185–218. https://doi.org/10.21894/jopr.2022.0036

• Pham, M. T., Huang, C. M., & Kirschner, R. (2019). First report of the oil palm disease fungus Marasmius palmivorus from Taiwan causing stem rot disease on native Formosa palm Arenga engleri as new host. Letters in Applied Microbiology, 70(3), 143-150. https://doi.org/10.1111/lam.13257

• Podder, D., & Ghosh, S. K. (2019). A new application of Trichoderma asperellum as an Anopheline larvicide for eco friendly management in medical science. Scientific Reports, 9(1), Article 1108. https://doi.org/10.1038/s41598-018-37108-2

• Rahman, M. M., Lourenço, M., Hassim, H. A., Baars, J. J., Sonnenberg, A. S., Cone, J. W., Boever, J. D., & Fievez, V. (2011). Improving ruminal degradability of oil palm fronds using white rot fungi. Animal Feed Science and Technology, 169(3-4), 157–166. https://doi.org/10.1016/j.anifeedsci.2011.06.014

• Raju, B., Santhanakumar, K. S., & Kesavachandran, U. (2020). Gastrointestinal involvement of unusual Mucormycete, Syncephalastrum racemosum in a diabetic patient with adenocarcinoma: Rare case presentation with review of literature. Infection, 48, 791–797. https://doi.org/10.1007/s15010-020-01455-y

• Rouches, E., Herpoël-Gimbert, I., Steyer, J. P., & Carrere, H. (2016). Improvement of anaerobic degradation by white-rot fungi pretreatment of lignocellulosic biomass: A review. Renewable and Sustainable Energy Reviews, 59, 179–198. https://doi.org/10.1016/j.rser.2015.12.317

• Rusli, N. D., Azmi, M. A., Mat, K., Hasnita, C. H., Wan-Zahari, M., Azhar, K., Zamri-Saad, M., & Hassim, H. A. (2019). The effect of physical and biological pre-treatments of oil palm fronds on in vitro ruminal degradability. Pertanika Journal of Tropical Agricultural Science, 42(2), 791-805.

• Rusli, N. D., Ghani, A. A. A., Mat, K., Yusof, M. T., Zamri-Saad, M., & Hassim, H. A. (2021). The potential of pretreated oil palm frond in enhancing rumen degradability and growth performance: A review. Advances in Animal and Veterinary Sciences, 9(6), 811–822. http://dx.doi.org/10.17582/journal.aavs/2021/9.6.811.822

• Saha, B. C., Qureshi, N., Kennedy, G. J., & Cotta, M. A. (2016). Biological pretreatment of corn stover with white-rot fungus for improved enzymatic hydrolysis. International Biodeterioration & Biodegradation, 109, 29–35. https://doi.org/10.1016/j.ibiod.2015.12.020

• Saif, F. A., Yaseen, S. A., Alameen, A. S., Mane, S. B., & Undre, P. B. (2020). Identification of Penicillium species of fruits using morphology and spectroscopic methods. In Journal of Physics: Conference Series, 1644, Article 12019. https://doi.org/10.1088/1742-6596/1644/1/012019

• Saminathan, M., Mohamed, W. N. W., Noh, A. M., Ibrahim, N. A., Fuat, M. A., Ramiah, S. K., Chung, E. L. T., & Dian, N. L. H. M. (2012). Treated oil palm frond and its utilisation as an improved feedstuff for ruminants-An overview. Journal of Oil Palm Research, 34(4), 591–607. https://doi.org/10.21894/jopr.2021.0041

• Sigler, L., Bartley, J. R., Parr, D. H., & Morris, A. J. (1999). Maxillary Sinusitis Caused by Medusoid Form ofSchizophyllum commune. Journal of Clinical Microbiology, 37(10), 3395–3398.

• Sukri, S. M., Rahman, R. A., Illias, R. M., & Yaakob, H. (2014). Optimization of alkaline pretreatment conditions of oil palm fronds in improving the lignocelluloses contents for reducing sugar production. Biotechnology Letter, 19(1), 9006–9018.

• Tamur, H. A., Al-Janabi, H. J., Al-Janabi, J. K. A., Mohsin, L. Y., & Al-Yassiry, Z. A. N. (2019). Characterization and antagonistic activity of new causal agent of wilt disease in Imperata cylindrica (Marasmius palmivorus). Journal of Pure and Applied Microbiology, 13(3), 1525–1536. https://doi.org/10.22207/JPAM.13.3.24

• Tian, X. F., Fang, Z., & Guo, F. (2012). Impact and prospective of fungal pre‐treatment of lignocellulosic biomass for enzymatic hydrolysis. Biofuels, Bioproducts and Biorefining, 6(3), 335–350. https://doi.org/10.1002/bbb.346

• Toth, G. B., & Pavia, H. (2000). Removal of dissolved brown algal phlorotannins using insoluble polyvinylpolypyrrolidone (PVPP). Journal of Chemical Ecology, 27, 1899–1910. https://doi.org/10.1023/A:1010421128190

• Tuyen, D. V., Phuong, H. N., Cone, J. W., Baars, J. J. P., Sonnenberg, A. S. M., & Hendriks, W. H. (2013). Effect of fungal treatments of fibrous agricultural by-products on chemical composition and in vitro rumen fermentation and methane production. Bioresource Technology, 129, 256–263. https://doi.org/10.1016/j.biortech.2012.10.128

• Verma, M., Brar, S. K., Tyagi, R. D., Surampalli, R. Y., & Val, J. R. (2007). Antagonistic fungi, Trichoderma spp. Panoply of Biological Control, 37, 1–20. https://doi.org/10.1016/j.bej.2007.05.012

• Walther, G., Pawłowska, J., Alastruey-Izquierdo, A., Wrzosek, M., Rodriguez-Tudela, J. L., Dolatabadi, S., Chakrabarti, A., & Hoog, G. S. D. (2013). DNA barcoding in Mucorales: An inventory of biodiversity. Persoonia: Molecular Phylogeny and Evolution of Fungi, 30(1), 11-47. https://doi.org/10.3767/003158513X665070

• Wang, F., Xu, L., Zhao, L., Ding, Z., Ma, H., & Terry, N. (2019). Fungal laccase production from lignocellulosic agricultural wastes by solid-state fermentation: A review. Microorganisms, 7(12), Article 665. https://doi.org/10.3390/microorganisms7120665

• Zafar, A. M., Najma, S., Farhana, T., Shahlla, I., Safia, A., Iqbal, A. (2017). Detection of aflatoxins and use of scanning electron microscope for the identification of fungal species in some commonly used spices. Asian Journal of Plant Science and Research, 7(5), 64–73.