Lipid yields from oleaginous yeasts isolated from the north Peruvian Andes by culture media non-limiting nitrogen
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Abstract
Oleochemicals can be obtained from oily yeasts due to their ability to produce a high lipid content. This research aimed to isolate them from the North Peruvian Andes with a lipid content greater than 20%. They were identified by sequencing internal transcribed spacer regions ITS of conserved ribosomal DNA (rDNA), evaluate their growth kinetics, biomass and lipid yields, using culture media with C/N 100:1+xylose (MS-1-7) and 2:1+glucose (MS-2-7). Growth kinetics up to the maximum stationary phase was evaluated using the parameterized Gompertz type II model. Rhodotorula glutinis, R. mucilaginosa, and R. kratochvilovae were selected. The C/N ratio in the culture medium influenced growth kinetics, biomass and lipids yields. With MS-1-7, a high specific growth rate (?max) was obtained, reaching the stationary phase between 6 to 9 h and the highest lipid accumulation between 23.1% and 31.5%. With the MS-2-7 medium, maximum biomass value obtained in the stationary phase between 37 and 51 h, which generated the highest biomass yields at the end of the entire process and lipid yield of 4.65, 5.59, and 8.80 g L-1 in the strains mentioned. There is potential to obtain high lipid yields using a culture media non-limiting nitrogen, examining not only the C/N ratio. But also, the quantities, nature of the components, and type of oleaginous yeasts taking care to avoid a high carbon concentration to prevent the Cabtree effect.
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Keywords
Lipid yield, Limiting and Non-limiting nitrogen, Rhodotorula glutinis, Rhodotorula mucilaginosa, Rhodotorula kratochvilovae
References
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Ageitos, J.M., Vallejo, J.A., Veiga-Crespo, P., & Villa, T.G. (2011). Oily yeasts as oleaginous cell factories. Applied Microbiology and Biotechnology, 90(4), 1219-1227. https://doi.org/10.1007/s00253-011-3200-z
Braunwald, T., Schwemmlein, L., Graeff-Hönninger, S., French, W.T., Hernandez, R., Holmes, W.E., & Claupein, W. (2013). Effect of different C/N ratios on carotenoid and lipid production by Rhodotorula glutinis. Applied Microbiology and Biotechnology, 97(14), 6581-6588. https://doi.org/10.1007/s00253-013-5005-8
Buzzini, P., Branda, E., Goretti, M., & Turchetti, B. (2012). Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiology Ecology, 82(2), 217-241. https://doi.org/10.1111/j.1574-6941.2012.01348.x
Chang, S.W., Shieh, C.J., Lee, G.C., Akoh, C.C., & Shaw, J.F. (2006). Optimized Growth Kinetics of Pichia pastoris and Recombinant Candida rugosa LIP1 Production by RSM. Journal of Molecular Microbiology and Biotechnology, 11(1-2), 28-40. https://doi.org/10.1159/000092817
Christophe, G., Kumar, V., Nouaille, R., Gaudet, G., Fontanille, P., Pandey, A., Socco, C.R., & Larroche, C. (2012). Recent developments in microbial oils production: a possible alternative to vegetable oils for biodiesel without competition with human food? Brazilian Archives of Biology and Technology, 55(1), 29-46. https://doi.org/10.1590/s1516-89132012000100004
Dai, C. C., Tao, J., Xie, F., Dai, Y. J., & Zhao, M. (2007). Biodiesel generation from oleaginous yeast Rhodotorula glutinis with xylose assimilating capacity. African Journal of Biotechnology, 6(18), 2130-2134. https://doi.org/10.58 97/ajb2007.000-2331
Dey, P., & Maiti, M.K. (2013). Molecular characterization of a novel isolate of Candida tropicalis for enhanced lipid production. Journal of Applied Microbiology, 114(5), 1357-1368. https://doi.org/10.1111/jam.12133
Fujita, S.I., Senda, Y., Nakaguchi, S., & Hashimoto, T. (2001). Multiplex PCR Using Internal Transcribed Spacer 1 and 2 Regions for Rapid Detection and Identification of Yeast Strains. Journal of Clinical Microbiology, 39(10), 3617-3622. https://doi.org/10.1128/jcm.39.10.3617-3622.2 001
Gientka, I., Kieliszek, M., Jermacz, K., & B?a?ejak, S. (2017). Identification and Characterization of Oleaginous Yeast Isolated from Kefir and Its Ability to Accumulate Intracellular Fats in Deproteinated Potato Wastewater with Different Carbon Sources. Biomed Research International, 2017, 1-19. https://doi.org/10.1155/2017/6061042
Gupta, A., Joia, J., Sood, A., Sood, R., Sidhu, C., & Kaur, G. (2016). Microbes as Potential Tool for Remediation of Heavy Metals: A Review. Journal of Microbial & Biochemical Technology, 8(4). https://doi.org/10.4172/1948-594 8.1000310
Jiru, T.M., Groenewald, M., Pohl, C., Steyn, L., Kiggundu, N., & Abate, D. (2017). Optimization of cultivation conditions for biotechnological production of lipid by Rhodotorula kratochvilovae (syn, Rhodosporidium kratochvilovae) SY89 for biodiesel preparation. 3 Biotech, 7(2). https://doi.org/10.1007/s13205-017-0769-7
Karamerou, E.E., & Webb, C. (2019). Cultivation modes for microbial oil production using oleaginous yeasts – A review. Biochemical Engineering Journal, 151, 107322. https://doi.org/10.1016/j.bej.2019.107322
Kot, A.M., B?a?ejak, S., Kurcz, A., Gientka, I., & Kieliszek, M. (2016). Rhodotorula glutinis—potential source of lipids, carotenoids, and enzymes for use in industries. Applied Microbiology and Biotechnology, 100(14), 6103-6117. https://doi.org/10.1007/s00253-016-7611-8
Kot, A.M., B?a?ejak, S., Kieliszek, M., Gientka, I., & Bry?, J. (2019). Simultaneous Production of Lipids and Carotenoids by the Red Yeast Rhodotorula from Waste Glycerol Fraction and Potato Wastewater. Applied Biochemistry and Biotechnology, 189(2), 589-607. https://doi.org/10.1007/s12010-019-03023-z
Lopes, H.J.S., Bonturi, N., Kerkhoven, E.J., Miranda, E.A., & Lahtvee, P.J. (2020). C/N ratio and carbon source-dependent lipid production profiling in Rhodotorula toruloides. Applied Microbiology and Biotechnology, 104(6), 2639-2649. https://doi.org/10.1007/s00253-020-10386-5
Maina, S., Pateraki, C., Kopsahelis, N., Paramithiotis, S., Drosinos, E.H., Papanikolaou, S., & Koutinas, A. (2016). Microbial oil production from various carbon sources by newly isolated oleaginous yeasts. Engineering in Life Sciences, 17(3), 333-344. https://doi.org/10.1002/elsc.2015 00153
Meesters, P.A.E.P., Huijberts, G.N.M., & Eggink, G. (1996). High-cell-density cultivation of the lipid accumulating yeast Cryptococcus curvatus using glycerol as a carbon source. Applied Microbiology and Biotechnology, 45(5), 575-579. https://doi.org/10.1007/s002530050731
Muñoz-Silva, L., Olivera-Gonzales, P., Santillán-Torres, M., & Tamariz-Angeles, C. (2019). Microorganismos tolerantes a metales pesados del pasivo minero Santa Rosa, Jangas (Perú). Revista Peruana de Biología, 26(1), 109-118. https://doi.org/10.15381/rpb.v26i1.15914
Papanikolaou, S., & Aggelis, G. (2011). Lipids of oleaginous yeasts. Part I: Biochemistry of single cell oil production. European Journal of Lipid Science and Technology, 113(8), 1031-1051. https://doi.org/10.1002/ejlt.201100014
Patel, A., Karageorgou, D., Rova, E., Katapodis, P., Rova, U., Christakopoulos, P., & Matsakas, L. (2020). An Overview of Potential Oleaginous Microorganisms and Their Role in Biodiesel and Omega-3 Fatty Acid-Based Industries. Microorganisms, 8(3), 434. https://doi.org/10.3390/microorganisms8030434
Ratledge, C. (2002). Regulation of lipid accumulation in oleaginous microorganisms. Biochemical Society Transactions, 30(6), 1047-1050. https://doi.org/10.1042/bst0301047
Sierra, R.V. (2013). Produção de leveduras oleaginosas em meio de cultura contendo hidrolisado de bagaço de cana-de-açúcar. Repositorio. unicamp.br. http://repositorio.unicamp.br/bitstream/REPOSIP/266600/1/SierraAristizabal_RuthVeronica_M.pdf.
Sitepu, I.R., Sestric, R., Ignatia, L., Levin, D., German, J.B., & Gillies, L.A., Almada, L.A.G., & Boundy-Mills, K.L. (2013). Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Bioresource Technology, 144, 360-369. https://doi.org/10.1016/j.biortech.2013.0 6.047
Sitepu, I.R., Garay, L.A., Sestric, R., Levin, D., Block, D.E., German, J.B., & Boundy-Mills, K.L. (2014). Oleaginous yeasts for biodiesel: Current and future trends in biology and production. Biotechnology Advances, 32(7), 1336-1360. https://doi.org/10.1016/j.biotechadv.2014.08.0 03
Sláviková, E., & Vadkertiová, R. (2000). The occurrence of yeasts in the forest soils. Journal of Basic Microbiology, 40(3), 207-212. https://doi.org/10.1002/1521-4028(200007)40:3<207::aid-jobm207>3.0.co;2-h
Spagnuolo, M., Yaguchi, A., & Blenner, M. (2019). Oleaginous yeast for biofuel and oleochemical production. Current Opinion in Biotechnology, 57, 73-81. https://doi.org/10.1016/j.copbio.2019.02.011
Sreeharsha, R.V., & Mohan, S.V. (2020). Obscure yet Promising Oleaginous Yeasts for Fuel and Chemical Production. Trends in Biotechnology, 38(8), 873-887. https://doi.org/10.1016/j.tibtech.2020.02.004
Tchakouteu, S.S., Chatzifragkou, A., Kalantzi, O., Koutinas, A.A., Aggelis, G., & Papanikolaou, S. (2014). Oleaginous yeast Cryptococcus curvatus exhibits interplay between biosynthesis of intracellular sugars and lipids. European Journal of Lipid Science and Technology, 117(5), 657-672. https://doi.org/10.1002/ejlt.201400347
Tjørve, K.M.C., & Tjørve, E. (2017). The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family. PLOS ONE, 12(6), e0178691. https://doi.org/10.1371/journal.pone.0178691
Toju, H., Tanabe, A.S., Yamamoto, S., & Sato, H. (2012). High-Coverage ITS Primers for the DNA-Based Identification of Ascomycetes and Basidiomycetes in Environmental Samples. Plos ONE, 7(7), e40863. https://doi.org/10.1371/journal.pone.0040863
Vasconcelos, B., Teixeira, J.C., Dragone, G., & Teixeira, J.A. (2019). Oleaginous yeasts for sustainable lipid production—from biodiesel to surf boards, a wide range of “green” applications. Applied Microbiology and Biotechnology, 103(9), 3651-3667. https://doi.org/10.1007/s00253-019-09742-x
Wuczkowski, M., & Prillinger, H. (2004). Molecular identification of yeasts from soils of the alluvial forest national park along the river Danube downstream of Vienna, Austria (“Nationalpark Donauauen”). Microbiological Research, 159(3), 263-275. https://doi.org/10.1016/j.micre s.2004.05.001
Yen, H.W., Palanisamy, G., & Su, G.C. (2019). The Influences of Supplemental Vegetable Oils on the Growth and ?-carotene Accumulation of Oleaginous Yeast-Rhodotorula glutinis. Biotechnology and Bioprocess Engineering, 24(3), 522-528. https://doi.org/10.1007/s12257-019-0027-4
Yurkov, A.M., Kemler, M., & Begerow, D. (2012). Assessment of yeast diversity in soils under different management regimes. Fungal Ecology, 5(1), 24-35. https://doi.org/10.1016/j.funeco.2011.07.004
Zalar P., Gunde-Cimerman N. (2014) Cold-Adapted Yeasts in Arctic Habitats. In: Buzzini P., Margesin R. (eds) Cold-adapted Yeasts (pp. 49-74). Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39681-6_3
Zarli, A. (2020). Oleochemicals: all time players of green chemistry. Studies in Surface Science and Catalysis, 77-95. https://doi.org/10.1016/B978-0-444-64337-7.00006-9
Zhang, Y., Nielsen, J., & Liu, Z. (2021). Yeast based biorefineries for oleochemical production. Current Opinion in Biotechnology, 67, 26-34. https://doi.org/10.1016/j.copb io.2020.11.009
Ageitos, J.M., Vallejo, J.A., Veiga-Crespo, P., & Villa, T.G. (2011). Oily yeasts as oleaginous cell factories. Applied Microbiology and Biotechnology, 90(4), 1219-1227. https://doi.org/10.1007/s00253-011-3200-z
Braunwald, T., Schwemmlein, L., Graeff-Hönninger, S., French, W.T., Hernandez, R., Holmes, W.E., & Claupein, W. (2013). Effect of different C/N ratios on carotenoid and lipid production by Rhodotorula glutinis. Applied Microbiology and Biotechnology, 97(14), 6581-6588. https://doi.org/10.1007/s00253-013-5005-8
Buzzini, P., Branda, E., Goretti, M., & Turchetti, B. (2012). Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiology Ecology, 82(2), 217-241. https://doi.org/10.1111/j.1574-6941.2012.01348.x
Chang, S.W., Shieh, C.J., Lee, G.C., Akoh, C.C., & Shaw, J.F. (2006). Optimized Growth Kinetics of Pichia pastoris and Recombinant Candida rugosa LIP1 Production by RSM. Journal of Molecular Microbiology and Biotechnology, 11(1-2), 28-40. https://doi.org/10.1159/000092817
Christophe, G., Kumar, V., Nouaille, R., Gaudet, G., Fontanille, P., Pandey, A., Socco, C.R., & Larroche, C. (2012). Recent developments in microbial oils production: a possible alternative to vegetable oils for biodiesel without competition with human food? Brazilian Archives of Biology and Technology, 55(1), 29-46. https://doi.org/10.1590/s1516-89132012000100004
Dai, C. C., Tao, J., Xie, F., Dai, Y. J., & Zhao, M. (2007). Biodiesel generation from oleaginous yeast Rhodotorula glutinis with xylose assimilating capacity. African Journal of Biotechnology, 6(18), 2130-2134. https://doi.org/10.58 97/ajb2007.000-2331
Dey, P., & Maiti, M.K. (2013). Molecular characterization of a novel isolate of Candida tropicalis for enhanced lipid production. Journal of Applied Microbiology, 114(5), 1357-1368. https://doi.org/10.1111/jam.12133
Fujita, S.I., Senda, Y., Nakaguchi, S., & Hashimoto, T. (2001). Multiplex PCR Using Internal Transcribed Spacer 1 and 2 Regions for Rapid Detection and Identification of Yeast Strains. Journal of Clinical Microbiology, 39(10), 3617-3622. https://doi.org/10.1128/jcm.39.10.3617-3622.2 001
Gientka, I., Kieliszek, M., Jermacz, K., & B?a?ejak, S. (2017). Identification and Characterization of Oleaginous Yeast Isolated from Kefir and Its Ability to Accumulate Intracellular Fats in Deproteinated Potato Wastewater with Different Carbon Sources. Biomed Research International, 2017, 1-19. https://doi.org/10.1155/2017/6061042
Gupta, A., Joia, J., Sood, A., Sood, R., Sidhu, C., & Kaur, G. (2016). Microbes as Potential Tool for Remediation of Heavy Metals: A Review. Journal of Microbial & Biochemical Technology, 8(4). https://doi.org/10.4172/1948-594 8.1000310
Jiru, T.M., Groenewald, M., Pohl, C., Steyn, L., Kiggundu, N., & Abate, D. (2017). Optimization of cultivation conditions for biotechnological production of lipid by Rhodotorula kratochvilovae (syn, Rhodosporidium kratochvilovae) SY89 for biodiesel preparation. 3 Biotech, 7(2). https://doi.org/10.1007/s13205-017-0769-7
Karamerou, E.E., & Webb, C. (2019). Cultivation modes for microbial oil production using oleaginous yeasts – A review. Biochemical Engineering Journal, 151, 107322. https://doi.org/10.1016/j.bej.2019.107322
Kot, A.M., B?a?ejak, S., Kurcz, A., Gientka, I., & Kieliszek, M. (2016). Rhodotorula glutinis—potential source of lipids, carotenoids, and enzymes for use in industries. Applied Microbiology and Biotechnology, 100(14), 6103-6117. https://doi.org/10.1007/s00253-016-7611-8
Kot, A.M., B?a?ejak, S., Kieliszek, M., Gientka, I., & Bry?, J. (2019). Simultaneous Production of Lipids and Carotenoids by the Red Yeast Rhodotorula from Waste Glycerol Fraction and Potato Wastewater. Applied Biochemistry and Biotechnology, 189(2), 589-607. https://doi.org/10.1007/s12010-019-03023-z
Lopes, H.J.S., Bonturi, N., Kerkhoven, E.J., Miranda, E.A., & Lahtvee, P.J. (2020). C/N ratio and carbon source-dependent lipid production profiling in Rhodotorula toruloides. Applied Microbiology and Biotechnology, 104(6), 2639-2649. https://doi.org/10.1007/s00253-020-10386-5
Maina, S., Pateraki, C., Kopsahelis, N., Paramithiotis, S., Drosinos, E.H., Papanikolaou, S., & Koutinas, A. (2016). Microbial oil production from various carbon sources by newly isolated oleaginous yeasts. Engineering in Life Sciences, 17(3), 333-344. https://doi.org/10.1002/elsc.2015 00153
Meesters, P.A.E.P., Huijberts, G.N.M., & Eggink, G. (1996). High-cell-density cultivation of the lipid accumulating yeast Cryptococcus curvatus using glycerol as a carbon source. Applied Microbiology and Biotechnology, 45(5), 575-579. https://doi.org/10.1007/s002530050731
Muñoz-Silva, L., Olivera-Gonzales, P., Santillán-Torres, M., & Tamariz-Angeles, C. (2019). Microorganismos tolerantes a metales pesados del pasivo minero Santa Rosa, Jangas (Perú). Revista Peruana de Biología, 26(1), 109-118. https://doi.org/10.15381/rpb.v26i1.15914
Papanikolaou, S., & Aggelis, G. (2011). Lipids of oleaginous yeasts. Part I: Biochemistry of single cell oil production. European Journal of Lipid Science and Technology, 113(8), 1031-1051. https://doi.org/10.1002/ejlt.201100014
Patel, A., Karageorgou, D., Rova, E., Katapodis, P., Rova, U., Christakopoulos, P., & Matsakas, L. (2020). An Overview of Potential Oleaginous Microorganisms and Their Role in Biodiesel and Omega-3 Fatty Acid-Based Industries. Microorganisms, 8(3), 434. https://doi.org/10.3390/microorganisms8030434
Ratledge, C. (2002). Regulation of lipid accumulation in oleaginous microorganisms. Biochemical Society Transactions, 30(6), 1047-1050. https://doi.org/10.1042/bst0301047
Sierra, R.V. (2013). Produção de leveduras oleaginosas em meio de cultura contendo hidrolisado de bagaço de cana-de-açúcar. Repositorio. unicamp.br. http://repositorio.unicamp.br/bitstream/REPOSIP/266600/1/SierraAristizabal_RuthVeronica_M.pdf.
Sitepu, I.R., Sestric, R., Ignatia, L., Levin, D., German, J.B., & Gillies, L.A., Almada, L.A.G., & Boundy-Mills, K.L. (2013). Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Bioresource Technology, 144, 360-369. https://doi.org/10.1016/j.biortech.2013.0 6.047
Sitepu, I.R., Garay, L.A., Sestric, R., Levin, D., Block, D.E., German, J.B., & Boundy-Mills, K.L. (2014). Oleaginous yeasts for biodiesel: Current and future trends in biology and production. Biotechnology Advances, 32(7), 1336-1360. https://doi.org/10.1016/j.biotechadv.2014.08.0 03
Sláviková, E., & Vadkertiová, R. (2000). The occurrence of yeasts in the forest soils. Journal of Basic Microbiology, 40(3), 207-212. https://doi.org/10.1002/1521-4028(200007)40:3<207::aid-jobm207>3.0.co;2-h
Spagnuolo, M., Yaguchi, A., & Blenner, M. (2019). Oleaginous yeast for biofuel and oleochemical production. Current Opinion in Biotechnology, 57, 73-81. https://doi.org/10.1016/j.copbio.2019.02.011
Sreeharsha, R.V., & Mohan, S.V. (2020). Obscure yet Promising Oleaginous Yeasts for Fuel and Chemical Production. Trends in Biotechnology, 38(8), 873-887. https://doi.org/10.1016/j.tibtech.2020.02.004
Tchakouteu, S.S., Chatzifragkou, A., Kalantzi, O., Koutinas, A.A., Aggelis, G., & Papanikolaou, S. (2014). Oleaginous yeast Cryptococcus curvatus exhibits interplay between biosynthesis of intracellular sugars and lipids. European Journal of Lipid Science and Technology, 117(5), 657-672. https://doi.org/10.1002/ejlt.201400347
Tjørve, K.M.C., & Tjørve, E. (2017). The use of Gompertz models in growth analyses, and new Gompertz-model approach: An addition to the Unified-Richards family. PLOS ONE, 12(6), e0178691. https://doi.org/10.1371/journal.pone.0178691
Toju, H., Tanabe, A.S., Yamamoto, S., & Sato, H. (2012). High-Coverage ITS Primers for the DNA-Based Identification of Ascomycetes and Basidiomycetes in Environmental Samples. Plos ONE, 7(7), e40863. https://doi.org/10.1371/journal.pone.0040863
Vasconcelos, B., Teixeira, J.C., Dragone, G., & Teixeira, J.A. (2019). Oleaginous yeasts for sustainable lipid production—from biodiesel to surf boards, a wide range of “green” applications. Applied Microbiology and Biotechnology, 103(9), 3651-3667. https://doi.org/10.1007/s00253-019-09742-x
Wuczkowski, M., & Prillinger, H. (2004). Molecular identification of yeasts from soils of the alluvial forest national park along the river Danube downstream of Vienna, Austria (“Nationalpark Donauauen”). Microbiological Research, 159(3), 263-275. https://doi.org/10.1016/j.micre s.2004.05.001
Yen, H.W., Palanisamy, G., & Su, G.C. (2019). The Influences of Supplemental Vegetable Oils on the Growth and ?-carotene Accumulation of Oleaginous Yeast-Rhodotorula glutinis. Biotechnology and Bioprocess Engineering, 24(3), 522-528. https://doi.org/10.1007/s12257-019-0027-4
Yurkov, A.M., Kemler, M., & Begerow, D. (2012). Assessment of yeast diversity in soils under different management regimes. Fungal Ecology, 5(1), 24-35. https://doi.org/10.1016/j.funeco.2011.07.004
Zalar P., Gunde-Cimerman N. (2014) Cold-Adapted Yeasts in Arctic Habitats. In: Buzzini P., Margesin R. (eds) Cold-adapted Yeasts (pp. 49-74). Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39681-6_3
Zarli, A. (2020). Oleochemicals: all time players of green chemistry. Studies in Surface Science and Catalysis, 77-95. https://doi.org/10.1016/B978-0-444-64337-7.00006-9
Zhang, Y., Nielsen, J., & Liu, Z. (2021). Yeast based biorefineries for oleochemical production. Current Opinion in Biotechnology, 67, 26-34. https://doi.org/10.1016/j.copb io.2020.11.009
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Lipid yields from oleaginous yeasts isolated from the north Peruvian Andes by culture media non-limiting nitrogen . (2021). Journal of Applied and Natural Science, 13(2), 607-615. https://doi.org/10.31018/jans.v13i2.2670
