Lipase production from Aniba canelilla endophytic fungi, characterization and application of the enzymatic extract

Authors

DOI:

https://doi.org/10.33448/rsd-v11i12.34326

Keywords:

Amazon; Endophyte; Biocatalysis; Endomelanconiopsis endophytica; Biodiesel.

Abstract

Endophytic fungi (EF) have a notable capacity to produce active molecules of industrial importance, such as hydrolytic enzymes. In this study we investigated the production of lipase by EFs isolated from the Amazonian species Aniba canelilla (Lauraceae), characterized the enzymatic extract obtained from the most promising fungus, and applied the lipolytic extract as a biocatalyst in the transesterification reaction for biodiesel production. The fungi were submitted to enzymatic screening in solid medium and in submerged fermentation to assess their lipase production. A total of 292 fungi were tested in solid media. Lipolytic activity was detected in 74% of the fungi cultivated in liquid media, 18 of which showing promising enzymatic production. The best lipase producer, Endomelanconiopsis endophytica QAT_7AC, was identified by sequencing of the ITS region. After adjusting the bioprocess conditions, E. endophytica QAT_7AC produced 2,415.5 U/mL of lipase after 72 h. The enzymatic extract showed higher lipolytic activity under pH 8.0 and 40 oC. The extract was applied as a biocatalyst in a transesterification reaction performed at 40 oC, with ethanol and waste cooking oil (3:1). The biodiesel yield was found to be 87% after 2 h rection when the fungal enzyme was used and 89% with the commercial biocatalyst. The endophytic fungi isolated from A. canelilla proved themselves to be biotechnologically relevant, as they can be explored as potential producers of lipases. The lipolytic extract can be applied in the synthesis of biodiesel using waste cooking oil.

Author Biographies

Rosiane Rodrigues Matias, Universidade do Estado do Amazonas

Graduate Program in Biodiversity and Biotechnology - Bionorte, School of Health Sciences

Juliana Gisele Corrêa Rodrigues, Universidade do Estado do Amazonas

Graduate Program in Biodiversity and Biotechnology - Bionorte, School of Health Sciences

Rudi Emerson de Lima Procópio, Universidade do Estado do Amazonas

Graduate Program in Biotechnology and Amazon Natural Resources, School of Health Sciences

Carla Roberta Matte, Federal University of Rio Grande do Sul

Laboratory of Biotechnology and Biochemistry Engineering, Institute of Science and Food Technology

Sergio Duvoisin Junior, Amazonas State University

Laboratory of Chemistry Applied to Technology, School of Technoloy

Marco Antonio Zachia Ayub, Federal University of Rio Grande do Sul

Laboratory of Biotechnology and Biochemistry Engineering, Institute of Science and Food Technology

Rosane Michele Duarte Soares, Federal University of Rio Grande do Sul

Laboratory of Polymeric Biomaterial, Institute of Chemistry

Patrícia Melchionna Albuquerque, Universidade do Estado do Amazonas

Graduate Program in Biodiversity and Biotechnology - Bionorte, School of Health Sciences

Graduate Program in Biotechnology and Amazon Natural Resources, School of Health Sciences

Laboratory of Chemistry Applied to Technology, School of Technology

References

A’Yuni, H., & Ilmi, M. (2021). Lipase production from Aspergillus aculeatus Ms.11 in broth medium with variation of agitation speed. AIP Conference Proceedings, 2353, 1–8. https://doi.org/10.1063/5.0052540

Al-Zaban, M. I., AlHarbi, M. A., Mahmoud, M. A., & Bahatheq, A. M. (2021). Production of biodiesel from oleaginous fungal lipid using highly catalytic bimetallic gold-silver core-shell nanoparticle. Journal of Applied Microbiology, 132(1), 381–389. https://doi.org/10.1111/jam.15176

Alabdalall, A. H., Al-Anazi, N. A., Aldakheel, L. A., Amer, F. H. I., Aldakheel, F. A., Ababutain, I. M., Alghamdi, A. I., & Al-Khaldi, E. M. (2021). Application and characterization of crude fungal lipases used to degrade fat and oil wastes. Scientific Reports, 11(1), 1–10. https://doi.org/10.1038/s41598-021-98927-4

Ali, C. H., Qureshi, A. S., Mbadinga, S. M., Liu, J. F., Yang, S. Z., & Mu, B. Z. (2017). Biodiesel production from waste cooking oil using onsite produced purified lipase from Pseudomonas aeruginosa FW_SH-1: Central composite design approach. Renewable Energy, 109, 93–100. https://doi.org/10.1016/j.renene.2017.03.018

Amini, Z., Ong, H. C., Harrison, M. D., Kusumo, F., Mazaheri, H., & Ilham, Z. (2017). Biodiesel production by lipase-catalyzed transesterification of Ocimum basilicum L. (sweet basil) seed oil. Energy Conversion and Management, 132, 82–90. https://doi.org/10.1016/j.enconman.2016.11.017

Banhos, E. F. dos, Souza, A. Q. L. de, Andrade, J. C. de, Souza, A. D. L., Koolen, H. H. F., & Albuquerque, P. M. (2014). Endophytic fungi from Myrcia guianensis at the Brazilian Amazon: Distribution and bioactivity. Brazilian Journal of Microbiology, 45(1), 153–161. https://doi.org/10.1590/S1517-83822014005000027

Barros, I. B. De, Custódio, D. L., Andrade, M. C. de, Veiga Júnior, V. F. da, Silva Neto, A. J. da, & Bastos, I. N. (2018). The inhibitory action of Aniba canelilla (H. B. K.) Mez. extracts on the corrosion of carbon steel in hydrochloric acid medium. Materials Research, 21(5), 1–8. https://doi.org/10.1590/1980-5373-MR-2017-0786

Batista, B. N., Matias, R. R., Oliveira, R. L., & Albuquerque, P. M. (2022). Hydrolytic enzyme production from açai palm (Euterpe precatoria) endophytic fungi and characterization of the amylolytic and cellulolytic extracts. World Journal of Microbiology and Biotechnology, 38(2), 1–13. https://doi.org/10.1007/s11274-021-03217-w

Batista, B. N., Raposo, N. V. de M., & Silva, I. R. da. (2018). Isolamento e avaliação da atividade antimicrobiana de fungos endofíticos de açaizeiro. Revista Fitos, 12(2), 161–174. https://doi.org/10.5935/2446-4775.20180015

Bernardi-Wenzel, J., Siqueira, A. L., Burin, F. A. G., Hein, D. P. R., Da Silveira, J. A., & Romani, S. (2012). Isolation and antagonistic activity of endophytic fungi of soybean (Glycine max (L.) Merrill). SaBios-Revista de Saúde e Biologia, 7(3), 86–96.

Carvalho Neto, F. G. M. da R. (2013). Isolamento e clonagem do gene que codifica a lipase do fungo Endomelanconiopsis endophytica. In Dissertação. Mestrado em Biotecnologia e Recursos Naturais da Amazônia. Universidade do Estado do Amazonas.

Castellani, A. (1939). Viability of mold culture of fungi in destiled water. Journal of Tropical Medical and Hygiene, 42, 225.

Cavalcante, F. T. T., Neto, F. S., Rafael de Aguiar Falcão, I., Erick da Silva Souza, J., de Moura Junior, L. S., da Silva Sousa, P., Rocha, T. G., de Sousa, I. G., de Lima Gomes, P. H., de Souza, M. C. M., & dos Santos, J. C. S. (2021). Opportunities for improving biodiesel production via lipase catalysis. Fuel, 288. https://doi.org/10.1016/j.fuel.2020.119577

Chandra, P., Enespa, Singh, R., & Arora, P. K. (2020). Microbial lipases and their industrial applications: A comprehensive review. Microbial Cell Factories, 19(1), 1–42. https://doi.org/10.1186/s12934-020-01428-8

Douanla-Meli, C., & Scharnhorst, A. (2021). Palm foliage as pathways of pathogenic Botryosphaeriaceae fungi and host of new Lasiodiplodia species from Mexico. Pathogens, 10(10), 1–16. https://doi.org/10.3390/pathogens10101297

Fadiji, A. E., & Babalola, O. O. (2020). Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Frontiers in Bioengineering and Biotechnology, 8, 1–20. https://doi.org/10.3389/fbioe.2020.00467

Fan, X., Niehus, X., & Sandoval, G. (2012). Lipases and phospholipases. Methods in Molecular Biology, 471–483. https://doi.org/10.1007/978-1-61779-600-5

Ferreira, M. C., Vieira, M. de L. A., Zani, C. L., Alves, T. M. de A., Junior, P. A. S., Murta, S. M. F., Romanha, A. J., Gil, L. H. V. G., Carvalho, A. G. de O., Zilli, J. E., Vital, M. J. S., Rosa, C. A., & Rosa, L. H. (2015). Molecular phylogeny, diversity, symbiosis and discover of bioactive compounds of endophytic fungi associated with the medicinal Amazonian plant Carapa guianensis Aublet (Meliaceae). Biochemical Systematics and Ecology, 59, 36–44. https://doi.org/10.1016/j.bse.2014.12.017

Firdaus, M. Y., Brask, J., Nielsen, P. M., Guo, Z., & Fedosov, S. (2016). Kinetic model of biodiesel production catalyzed by free liquid lipase from Thermomyces lanuginosus. Journal of Molecular Catalysis B: Enzymatic, 133, 55–64. https://doi.org/10.1016/j.molcatb.2016.07.011

Gama, A. M. da. (2012). Prospecção, caracterização e purificação de lipase microbiana. In Dissertação. Mestrado em Biotecnologia e Recursos Naturais da

Amazônia. Universidade do Estado do Amazonas.

Giongo, J. L., Vaucher, R. A., Da Silva, A. S., Oliveira, C. B., de Mattos, C. B., Baldissera, M. D., Sagrillo, M. R., Monteiro, S. G., Custódio, D. L., Souza de Matos, M., Sampaio, P. T., Teixeira, H. F., Koester, L. S., & da Veiga Junior, V. F. (2017). Trypanocidal activity of the compounds present in Aniba canelilla oil against Trypanosoma evansi and its effects on viability of lymphocytes. Microbial Pathogenesis, 103, 13–18. https://doi.org/10.1016/j.micpath.2016.12.006

Gomes, E. M. C., & Pena, R. da C. M. (2016). Isolamento, Caracterização morfológica e avaliação do crescimento micelial e esporulação em diferentes meios de cultura de cepas do fungo Quambalaria sp. Biota Amazônia, 6(4), 59–63. https://doi.org/10.18561/2179-5746/biotaamazonia.v6n4p59-63

Guo, J., Sun, S., & Liu, J. (2020). Conversion of waste frying palm oil into biodiesel using free lipase a from Candida antarctica as a novel catalyst. Fuel, 267, 117323. https://doi.org/10.1016/j.fuel.2020.117323

Hawksworth, D. L., & Lücking, R. (2017). Fungal diversity revisited: 2.2 to 3.8 million species. The Fungal Kingdom, 79–95. https://doi.org/10.1128/9781555819583.ch4

Huang, L., Zheng, D., Zhao, Y., Ma, J., Li, Y., Xu, Z., Shan, M., Shao, S., Guo, Q., Zhang, J., Lu, F., & Liu, Y. (2019). Improvement of the alkali stability of Penicillium cyclopium lipase by error-prone PCR. Electronic Journal of Biotechnology, 39, 91–97. https://doi.org/10.1016/j.ejbt.2019.04.002

IAL, I. A. L. (2008). Métodos físico-químicos para análises de alimentos (1st Digita).

Karimi, M. (2016). Immobilization of lipase onto mesoporous magnetic nanoparticles for enzymatic synthesis of biodiesel. Biocatalysis and Agricultural Biotechnology, 8, 182–188. https://doi.org/10.1016/j.bcab.2016.09.009

Krishnan, A., Convey, P., Gonzalez-Rocha, G., & Alias, S. A. (2016). Production of extracellular hydrolase enzymes by fungi from King George Island. Polar Biology, 39(1), 65–76. https://doi.org/10.1007/s00300-014-1606-7

Kumar, D., Banerjee, A., & Singh, B. (2021). Chapter 1 - Biocatalysis in industrial biodiesel and bioethanol production. In Inamuddin, R. Boddula, M. I. Ahamed, & Abdull (Eds.), Green Sustainable Process for Chemical and Environmental Engineering and Science (pp. 1–28). Elsevier. https://doi.org/https://doi.org/10.1016/B978-0-12-819721-9.00007-8

Leung, D. Y. C., & Guo, Y. (2006). Transesterification of neat and used frying oil: Optimization for biodiesel production. Fuel Processing Technology, 87(10), 883–890. https://doi.org/10.1016/j.fuproc.2006.06.003

Matias, R. R., Sepúlveda, A. M. G., Batista, B. N., de Lucena, J. M. V. M., & Albuquerque, P. M. (2021). Degradation of Staphylococcus aureus biofilm using hydrolytic enzymes produced by Amazonian endophytic fungi. Applied Biochemistry and Biotechnology, 193(7), 2145–2161. https://doi.org/10.1007/s12010-021-03542-8

Mehmood, U., Muneer, F., Riaz, M., Sarfraz, S., & Nadeem, H. (2021). Biocatalytic processes for biodiesel production. In R. Inamuddin, M. Ahamed, R. Bodulla, & M. Rezakazemi (Eds.), Biodiesel Technology and Applications (pp. 1–58).

Monteiro, M. C. P., Tavares, D. G., Nery, E. M., de Queiroz, M. V., Pereira, O. L., & Cardoso, P. G. (2020). Enzyme production by Induratia spp. isolated from coffee plants in Brazil. Brazilian Archives of Biology and Technology, 63, 1–9. https://doi.org/10.1590/1678-4324-2020180673

Muanruksa, P., & Kaewkannetra, P. (2020). Combination of fatty acids extraction and enzymatic esterification for biodiesel production using sludge palm oil as a low-cost substrate. Renewable Energy, 146, 901–906. https://doi.org/10.1016/j.renene.2019.07.027

Nagel, J. H., Wingfield, M. J., & Slippers, B. (2021). Increased abundance of secreted hydrolytic enzymes and secondary metabolite gene clusters define the genomes of latent plant pathogens in the Botryosphaeriaceae. BMC Genomics, 22(1), 1–24. https://doi.org/10.1186/s12864-021-07902-w

Nascimento, C. S., Dos Santos, V. L., & Andrade, M. H. C. de. (2014). Análise da produção de protease e lipase por fungos filamentosos isolados do fruto da macaúba (Acrocomia aculeata (Jacq) Lood. Ex Mart). XX Congresso Brasileiro de Engenharia Química, 1–8. https://doi.org/10.5151/chemeng-cobeq2014-0222-26465-171722

Nascimento, J. S., Silva, F. M., Magallanes-Noguera, C. A., Sanz, M. K., Santos, E. G. dos, Caldas, I. S., Luiz, J. H. H., & Silva, E. de O. (2020). Natural trypanocidal product produced by endophytic fungi through co-culturing. Folia Microbiologica, 65(2), 323–328. https://doi.org/10.1007/s12223-019-00727-x

Nayana, P., Aiswarya, C., Aparna, C. K., & Nambisan, P. (2020). Dataset on optimization of lignin peroxidase production by Endomelanconiopsis sp. under submerged fermentation using one factor at a time approach. Data in Brief, 29, 105244. https://doi.org/10.1016/j.dib.2020.105244

Naylor, R. L., & Higgins, M. M. (2018). The rise in global biodiesel production: Implications for food security. Global Food Security, 16, 75–84. https://doi.org/10.1016/j.gfs.2017.10.004

Oliveira-Bouzas, V., Pita-Calvo, C., Lourdes Vázquez-Odériz, M., & Ángeles Romero-Rodríguez, M. (2021). Evaluation of a modified atmosphere packaging system in pallets to extend the shelf-life of the stored tomato at cooling temperature. Food Chemistry, 364, 130309. https://doi.org/10.1016/j.foodchem.2021.130309

Oliveira Filho, A. A. de, Fernandes, H. M. B., & Assis, T. J. C. F. (2015). Lauraceae’s Family: A brief review of cardiovascular effects. International Journal of Pharmacognosy and Phytochemical Research, 7(1), 22–26.

Oliveira, G. F., Silva, M. R. L., & Hirata, D. B. (2021). Production of new lipase from Preussia africana and partial characterization. Preparative Biochemistry and Biotechnology, 2021 1–8. https://doi.org/10.1080/10826068.2021.2012684

Palanichamy, P., Krishnamoorthy, G., Kannan, S., & Marudhamuthu, M. (2018). Egyptian journal of basic and applied sciences bioactive potential of secondary metabolites derived from medicinal plant endophytes. Egyptian Journal of Basic and Applied Sciences, 5(4), 303–312. https://doi.org/10.1016/j.ejbas.2018.07.002

Putri, D. N., Khootama, A., Perdani, M. S., Utami, T. S., & Hermansyah, H. (2020). Optimization of Aspergillus niger lipase production by solid state fermentation of agro-industrial waste. Energy Reports, 6, 331–335. https://doi.org/10.1016/j.egyr.2019.08.064

Rattanavipanon, W., Nithiphongwarakul, C., Sirisuwansith, P., Chaiyasothi, T., Thakkinstian, A., Nathisuwan, S., & Pathomwichaiwat, T. (2021). Effect of tomato, lycopene and related products on blood pressure: A systematic review and network meta-analysis. Phytomedicine, 88, 153512. https://doi.org/10.1016/j.phymed.2021.153512

Rojas, E. I., Herre, E. A., Mej́ia, L. C., Arnold, A. E., Chaverri, P., & Samuels, G. J. (2008). Endomelanconiopsis, a new anamorph genus in the Botryosphaeriaceae. Mycologia, 100(5), 760–775. https://doi.org/10.3852/07-207

Romão, T. C., Menezes Filho, A. C. P., Tininis, A. G., Oliveira, M. S., Felippe, L. G., Castro, C. F. S., Morais, P. B. (2022). Fungal amylases applied to the sweet potato starch for bioethanol production. Research, Society and Development, 11(10), e136111032583. https://doi.org/10.33448/rsd-v11i10.32583.

Romão, T. C., Menezes-Filho, A. C. P., Harakava, R., Castro, C. F. S., & Morais, P. B. (2024). Molecular and morphological diversity, qualitative chemical profile and antioxidant activity of filamentous fungi of the digestive tract of Phylloicus sp. (Trichoptera: Calamoceratidae). Brazilian Journal of Biology, 84, e259983. https://doi.org/10.1590/1519-6984.259983

Rossi, G. Z. De, Borges, I. R., Perego, T. F., Toledo, V. D. M., & Ferreira, L. F. P. (2018). Análise técnica da produção do biodiesel a partir do óleo de fritura residual. The Journal of Engineering and Exact Sciences, 4(1), 0101–0108. https://doi.org/10.18540/jcecvl4iss1pp0101-0108

Roy, M., Kumar, R., Ramteke, A., & Sit, N. (2018). Identification of lipase producing fungus isolated from dairy waste contaminated soil and optimization of culture conditions for lipase production by the isolated fungus. Journal of Microbiology, Biotechnology and Food Sciences, 8(1), 698–704. https://doi.org/10.15414/jmbfs.2018.8.1.698-704

Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual (2nd ed.). Cold Spring Harbor Laboratory Press.

Shepherd, T., Robertson, G. W., Griffiths, D. W., Birch, A. N. E., & Duncan, G. (1995). Effects of environment on the composition of epicuticular wax esters from kale and swede. Phytochemistry, 40(2), 407–417. https://doi.org/10.1016/S0031-9422(97)00272-0

Silva, T. A. C. e, Souza, C. R. F., Oliveira, W. P., & Said, S. (2014). Characterization and spray drying of lipase produced by the endophytic fungus Cercospora kikuchii. Brazilian Journal of Chemical Engineering, 31(4), 849–858. https://doi.org/10.1590/0104-6632.20140314s00002880

Soldi, E., Casey, C., Murphy, B. R., & Hodkinson, T. R. (2020). Fungal endophytes for grass-based bioremediation: An endophytic consortium isolated from Agrostis stolonifera stimulates the growth of Festuca arundinacea in lead contaminated soil. Journal of Fungi, 6(4), 1–15. https://doi.org/10.3390/jof6040254

Sopalun, K., & Iamtham, S. (2020). Isolation and screening of extracellular enzymatic activity of endophytic fungi isolated from Thai orchids. South African Journal of Botany, 134, 273–279. https://doi.org/10.1016/j.sajb.2020.02.005

Souza-Junior, F. J. C., Luz-Moraes, D., Pereira, F. S., Barros, M. A., Fernandes, L. M. P., Queiroz, L. Y., Maia, C. F., Maia, J. G. S., & Fontes-Junior, E. A. (2020). Aniba canelilla (Kunth) Mez (Lauraceae): A review of ethnobotany, phytochemical, antioxidant, anti-inflammatory, cardiovascular, and neurological properties. Frontiers in Pharmacology, 11, 1–14. https://doi.org/10.3389/fphar.2020.00699

Souza, B. dos S., Oliveira, D. R. de, Rocha, F. V. R. da, Canto, E. S. M., Oliveira, D. P. de, & Dos Santos, T. T. (2018). Endophytic fungi associated with the medicinal plant Kalanchoe pinnata (Lam.) Pers. DESAFIOS - Revista Interdisciplinar da Universidade Federal do Tocantins, 5(3), 30–45. https://doi.org/10.20873/uft.2359-3652.2018v5n3p30

Talukder, M. M. R., Wu, J. C., Fen, N. M., & Melissa, Y. L. S. (2010). Two-step lipase catalysis for production of biodiesel. Biochemical Engineering Journal, 49(2), 207–212. https://doi.org/10.1016/j.bej.2009.12.015

Thapa, S., Li, H., Ohair, J., Bhatti, S., Chi, F., Kamal, C., Nasr, A., & Johnson, T. (2019). Biochemical characteristics of microbial enzymes and their significance from industrial perspectives. Molecular Biotechnology, 61(8), 579–601. https://doi.org/10.1007/s12033-019-00187-1

Vélez-Terreros, P. Y., Romero-Estévez, D., Yánez-Jácome, G. S., Simbaña-Farinango, K., & Navarrete, H. (2021). Comparison of major nutrients and minerals between organic and conventional tomatoes. A review. Journal of Food Composition and Analysis, 100, 103922 https://doi.org/10.1016/j.jfca.2021.103922

Winkler, U. K., & Stuckmann, M. (1979). Glycogen, hyaluronate, and some other polysaccharides greatly enhance the formation of exolipase by Serratia marcescens. Journal of Bacteriology, 138(3), 663–670.

Zanotto, S. P., Romano, I., Lisboa, L. U. S., Duvoisin Jr, S., Martins, M. K., Lima, F. A., Silva, S. F., & Albuquerque, P. M. (2009). Potential application in biocatalysis of mycelium-bound lipases from Amazonian Fungi. Journal Brazilian Chemical Society, 20(6), 1046–1059. https://doi.org/10.1590/S0103-50532009000600008

Downloads

Published

10/09/2022

How to Cite

MATIAS, R. R.; RODRIGUES, J. G. C.; PROCÓPIO, R. E. de L.; MATTE, C. R. .; DUVOISIN JUNIOR, S.; AYUB, M. A. Z.; SOARES, R. M. D.; ALBUQUERQUE, P. M. Lipase production from Aniba canelilla endophytic fungi, characterization and application of the enzymatic extract. Research, Society and Development, [S. l.], v. 11, n. 12, p. e180111234326, 2022. DOI: 10.33448/rsd-v11i12.34326. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/34326. Acesso em: 4 nov. 2024.

Issue

Section

Agrarian and Biological Sciences