Produção ecologicamente correta de ácidos graxos nutracêuticos e cosmecêuticos pelo fungo oleaginoso Lichtheimia hyalospora UCP 1266 usando substratos renováveis
DOI:
https://doi.org/10.33448/rsd-v11i8.30753Palavras-chave:
Lipídeos microbianos; Fungos Mucorales; Glicerol bruto; Milhocina; Resíduos agroindustriais.Resumo
Os ácidos graxos poliinsaturados (AGPIs) são essenciais para as funções humanas e podem ser utilizados em nutracêuticos; no entanto, as fontes tradicionais são ambientalmente insustentáveis. Uma estratégia promissora para reduzir os custos de produção dos AGPIs é a utilização de fontes agroindustriais econômicas como substratos nos meios de cultura para micro-organismos oleaginosos. Neste estudo, investigamos o potencial do fungo Lichtheimia hyalospora UCP 1266 (isolado do solo da Caatinga, Brasil) na produção de AGPIs, através da conversão metabólica dos substratos alternativos glicerol bruto e milhocina. O cultivo de L. hyalospora UCP 1266 em meio com glicose (Meio Sintético para Mucorales - SMM) rendeu 2,1 g/L de biomassa e 0,6 g/L de lipídeos totais. No entanto, no ensaio 4 do planejamento fatorial completo de 22, com glicerol bruto 8% e milhocina 8%, proporcionou maior rendimento de biomassa (15,5 g/L) e lipídios totais (12,8 g/L). Os lipídios produzidos neste meio apresentaram composição de ácidos graxos saturados, monoinsaturados e poliinsaturados (AGS=35,13%, AGMIs=46,09% e AGPIs=18,14%). O micro-organismo mostrou-se promissor na produção de ômega 6 (ácido linoleico, C18:2), ácido γ-linolênico (C18:3), ômega 3 (ácido α-linolênico, C18:3) e ômega 9 (ácido oleico, C18:1). Os resultados indicaram L. hyalospora UCP 1266 como fungo oleaginoso com grande potencial de uso no desenvolvimento de ingredientes nutracêuticos para alimentos ou aplicado em cosmecêuticos e/ou nutricosméticos.
Referências
Aburto, J. M., Schöley, J., Kashnitsky, I., Zhang, L., Rahal, C., Missov, T. I., ... & Kashyap, R. (2022). Quantifying impacts of the COVID-19 pandemic through life-expectancy losses: a population-level study of 29 countries. International journal of epidemiology, 51(1), 63-74.
Alastruey-Izquierdo, A., Hoffmann, K., de Hoog, G. S., Rodriguez-Tudela, J. L., Voigt, K., Bibashi, E., & Walther, G. (2010). Species recognition and clinical relevance of the zygomycetous genus Lichtheimia (syn. Absidia pro parte, Mycocladus). Journal of Clinical Microbiology, 48(6), 2154-2170.
Alonso, D. L., & Maroto, F. G. (2000). Plants as ‘chemical factories’ for the production of polyunsaturated fatty acids. Biotechnology advances, 18(6), 481-497.
Arbex, A. K., Bizarro, V. R., Santos, J. C. S., Araújo, L. M. M., de Jesus, A. L. C., Fernandes, M. S. A., ... & Marcadenti, A. (2015). The impact of the essential fatty acids (EFA) in human health. Open Journal of Endocrine and Metabolic Diseases, 5(07), 98.
Asher, A., Tintle, N. L., Myers, M., Lockshon, L., Bacareza, H., & Harris, W. S. (2021). Blood omega-3 fatty acids and death from COVID-19: A pilot study. Prostaglandins, Leukotrienes and Essential Fatty Acids, 166, 102250.
Athenaki, M., Gardeli, C., Diamantopoulou, P., Tchakouteu, S. S., Sarris, D., Philippoussis, A., & Papanikolaou, S. (2018). Lipids from yeasts and fungi: physiology, production and analytical considerations. Journal of Applied Microbiology, 124(2), 336-367.
Béligon, V., Christophe, G., Fontanille, P., & Larroche, C. (2016). Microbial lipids as potential source to food supplements. Current Opinion in Food Science, 7, 35-42.
Bellou, S., Triantaphyllidou, I. E., Aggeli, D., Elazzazy, A. M., Baeshen, M. N., & Aggelis, G. (2016). Microbial oils as food additives: recent approaches for improving microbial oil production and its polyunsaturated fatty acid content. Current opinion in Biotechnology, 37, 24-35.
Bellou, S.; Makri, A., Sarris, D., Michos, K., Rentoumi, P., Celik, A., Aggelis, G. (2014). The olive mill wastewater as substrate for single cell oil production by Zygomycetes. Journal of Biotechnology. 170: 50-59.
Berger, L. R. R., Stamford, T. C. M., Stamford-Arnaud, T. M., de Oliveira Franco, L., Do Nascimento, A. E., Cavalcante, H. M. D. M., ... & Maria, G. (2014). Effect of corn steep liquor (CSL) and cassava wastewater (CW) on chitin and chitosan production by Cunninghamella elegans and their physicochemical characteristics and cytotoxicity. Molecules, 19(3), 2771-2792.
Cardoso, A., Lins, C. I. M., Dos Santos, E. R., Silva, M. C. F., & Campos-Takaki, G. M. (2012). Microbial enhance of chitosan production by Rhizopus arrhizus using agroindustrial substrates. Molecules, 17(5), 4904-4914.Carvalho, A. K.; Rivaldi, J. D.; Barbosa, J. C.; de Castro, H. F. Biosynthesis, characterization and enzymatic transesterification of single cell oil of Mucor circinelloides–A sustainable pathway for biofuel production. Biores. technol. 2015. 181, 47-53. https://doi.org/10.1016/j.biortech.2014.12.110
Castanha, R. F., Mariano, A. P., Morais, L. A. S. D., Scramin, S., & Monteiro, R. T. R. (2014). Optimization of lipids production by Cryptococcus laurentii 11 using cheese whey with molasses. Brazilian Journal of Microbiology, 45(2), 379-387.
Čertík, M., Berhan, S. S., & Šajbidor, J. (1993). Lipid production and fatty acid composition of selected strains belonging to Mucorales. Acta biotechnologica, 13(2), 193-196.
Chatzifragkou, A., Makri, A., Belka, A., Bellou, S., Mavrou, M., Mastoridou, M., ... & Papanikolaou, S. (2011). Biotechnological conversions of biodiesel derived waste glycerol by yeast and fungal species. Energy, 36(2), 1097-1108.
Cicero, A. F., Nascetti, S., López-Sabater, M. C., Elosua, R., Salonen, J. T., Nyyssonen, K., ... & EUROLIVE Study Group. (2008). Changes in LDL fatty acid composition as a response to olive oil treatment are inversely related to lipid oxidative damage: The EUROLIVE study. Journal of the American College of Nutrition, 27(2), 314-320.
de Souza Mendonça, R., Sá, A. V. P., Rosendo, L. A., dos Santos, R. A., do Amaral Marques, N. S. A., Souza, A. F., ... & de Campos Takaki, G. M. (2021). Produção de biossurfactante e lipídeos por uma nova cepa de Absidia cylindrospora UCP 1301 isolada do solo da Caatinga usando subprodutos agroindustriais de baixo custo. Brazilian Journal of Development, 7(1), 8300-8313.
de Souza, A. F., Galindo, H. M., de Lima, M. A. B., Ribeaux, D. R., Rodríguez, D. M., da Silva Andrade, R. F., ... & de Campos-Takaki, G. M. (2020). Biotechnological strategies for chitosan production by mucoralean strains and dimorphism using renewable substrates. International Journal of Molecular Sciences, 21(12), 4286.
Dimitrijevic, M. V., Mitic, V. D., Jovanovic, O. P., Stankov Jovanovic, V. P., Nikolic, J. S., Petrovic, G. M., & Stojanovic, G. S. (2018). Comparative study of fatty acids profile in eleven wild mushrooms of Boletacea and Russulaceae families. Chemistry & Biodiversity, 15(1), e1700434
Diwan, B., Parkhey, P., & Gupta, P. (2018). From agro-industrial wastes to single cell oils: a step towards prospective biorefinery. Folia microbiologica, 63(5), 547-568.
Domingo, J. L., Bocio, A., Falcó, G., & Llobet, J. M. (2007). Benefits and risks of fish consumption: Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology, 230(2-3), 219-226.
Durham, D. R., and Kloos, W. E. (1978). Comparative Study of the Total Cellular Fatty Acids of Staphylococcus Species of Human Origin. International Journal of Systematic and Evolutionary Microbiology, 28 (2): 223-228.
Elias, P. M., Brown, B. E., & Ziboh, V. A. (1980). The permeability barrier in essential fatty acid deficiency: evidence for a direct role for linoleic acid in barrier function. Journal of Investigative Dermatology, 74(4), 230-233.
Fakas, S., Makri, A., Bellou, S., & Aggelis, G. (2009). Pathways to aerobic glycerol catabolism and their regulation. Microbial conversions of raw glycerol, 9, 18.
Fazili, A. B. A., Shah, A. M., Zan, X., Naz, T., Nosheen, S., Nazir, Y., ... & Song, Y. (2022). Mucor circinelloides: a model organism for oleaginous fungi and its potential applications in bioactive lipid production. Microbial cell factories, 21(1), 1-19.
Further, T. (2009). Mycological Research News. Journal of the Linnean Society, 155, 449-456.
Galán, B., Santos-Merino, M., Nogales, J., De la Cruz, F., & García, J. L. (2020). Microbial oils as nutraceuticals and animal feeds. Health consequences of microbial interactions with hydrocarbons, oils, and lipids, 401-445.
Hansen, H. S., & Jensen, B. (1985). Essential function of linoleic acid esterified in acylglucosylceramide and acylceramide in maintaining the epidermal water permeability barrier. Evidence from feeding studies with oleate, linoleate, arachidonate, columbinate and α-linolenate. Biochimica et Biophysica Acta (BBA)-Lipids and Lipid Metabolism, 834(3), 357-363.
Hashem, A. H., Hasanin, M. S., Khalil, A. M. A., & Suleiman, W. B. (2020). Eco-green conversion of watermelon peels to single cell oils using a unique oleaginous fungus: Lichtheimia corymbifera AH13. Waste and Biomass Valorization, 11(11), 5721-5732.
Hesseltine, C. W., & Ellis, J. J. (1966). Species of Absidia with ovoid sporangiospores. I. Mycologia, 58(5), 761-785.
Hesseltine, C. W., & Anderson, R. F. (1957). Microbiological production of carotenoids. I. Zygospores and carotene produced by intraspecific and interspecific crosses of Choanephoraceae in liquid media. Mycologia, 49(4), 449-452.
Hoffmann, K., Walther, G., & Voigt, K. (2009). Mycocladus vs. Lichtheimia: a correction (Lichtheimiaceae fam. nov., Mucorales, Mucoromycotina). Mycol Res, 113(3), 277-8.
Hoffmann, K., & Voigt, K. (2009). Absidia parricida plays a dominant role in biotrophic fusion parasitism among mucoralean fungi (Zygomycetes): Lentamyces, a new genus for A. parricida and A. zychae. Plant Biology, 11(4), 537-554.
Hoffmann, K. (2010). Identification of the genus Absidia (Mucorales, Zygomycetes): a comprehensive taxonomic revision. Molecular identification of fungi, 439-460.
Hoffmann, K., Discher, S., & Voigt, K. (2007). Revision of the genus Absidia (Mucorales, Zygomycetes) based on physiological, phylogenetic, and morphological characters; thermotolerant Absidia spp. form a coherent group, Mycocladiaceae fam. nov. Mycological research, 111(10), 1169-1183.
Hyde, K. D., Bahkali, A. H., & Moslem, M. A. (2010). Fungi—an unusual source for cosmetics. Fungal diversity, 43(1), 1-9
Kadhim, K. F., & Alrubayae, I. M. (2019). Study of lipase production and lipids accumulation of oleaginous fungi isolated from oil-rich soil in Basrah.
Kikukawa, H., Sakuradani, E., Ando, A., Shimizu, S., & Ogawa, J. (2018). Arachidonic acid production by the oleaginous fungus Mortierella alpina 1S-4: A review. Journal of advanced research, 11, 15-22.
Kosa, G., Zimmermann, B., Kohler, A., Ekeberg, D., Afseth, N. K., Mounier, J., & Shapaval, V. (2018). High-throughput screening of Mucoromycota fungi for production of low-and high-value lipids. Biotechnology for biofuels, 11(1), 1-17.
Kothri, M., Mavrommati, M., Elazzazy, A. M., Baeshen, M. N., Moussa, T. A., & Aggelis, G. (2020). Microbial sources of polyunsaturated fatty acids (PUFAs) and the prospect of organic residues and wastes as growth media for PUFA-producing microorganisms. FEMS Microbiology Letters, 367(5), fnaa028.
Lenihan-Geels, G., Bishop, K. S.;,Ferguson, L. R. (2013) Alternative sources of omega-3 fats: can we find a sustainable substitute for fish?. Nutrition ; 5(4): 1301-1315.
Li, W., Zheng, P., Guo, J., Ji, J., Zhang, M., Zhang, Z., ... & Abbas, G. (2014). Characteristics of self-alkalization in high-rate denitrifying automatic circulation (DAC) reactor fed with methanol and sodium acetate. Bioresource technology, 154, 44-50.
Lin, T. K., Zhong, L., & Santiago, J. L. (2017). Anti-inflammatory and skin barrier repair effects of topical application of some plant oils. International journal of molecular sciences, 19(1), 70.
Lowry, J. R., Marshall, N., Wenzel, T. J., Murray, T. E., & Klegeris, A. (2020). The dietary fatty acids α-linolenic acid (ALA) and linoleic acid (LA) selectively inhibit microglial nitric oxide production. Molecular and Cellular Neuroscience, 109, 103569.
Mack Correa, M. C., Mao, G., Saad, P., Flach, C. R., Mendelsohn, R., & Walters, R. M. (2014). Molecular interactions of plant oil components with stratum corneum lipids correlate with clinical measures of skin barrier function. Experimental dermatology, 23(1), 39-44.
Manocha, M. S., San-Blas, G., & Centeno, S. (1980). Lipid composition of Paracoccidioides brasiliensis: possible correlation with virulence of different strains. Microbiology, 117(1), 147-154.
Martins, M. B., Suaiden, A. S., Piotto, R. F., & Barbosa, M. (2008). Propriedades dos ácidos graxos poliinsaturados–Omega 3 obtidos de óleo de peixe e óleo de linhaça Properties of Omega-3 polyunsaturated fatty acids obtained of fish oil and flaxseed oil. Rev Inst Ciênc Saúde, 26(2), 153-6.
Nasr, M., Nahvi, I., Keyhanfar, M., & Mirbagheri, M. (2017). The effect of carbon and nitrogen sources on the fatty acids profile of Mortierella vinacea. Biological Journal of Microorganism, 5(20), 1-8.
Kannan, N., Rao, A. S., & Nair, A. (2021). Microbial production of omega‐3 fatty acids: an overview. Journal of Applied Microbiology, 131(5), 2114-2130.
Ochsenreither, K., Glück, C., Stressler, T., Fischer, L., & Syldatk, C. (2016). Production strategies and applications of microbial single cell oils. Frontiers in microbiology, 7, 1539.
Papanikolaou, S., Fakas, S., Fick, M., Chevalot, I., Galiotou-Panayotou, M., Komaitis, M., ... & Aggelis, G. (2008). Biotechnological valorisation of raw glycerol discharged after bio-diesel (fatty acid methyl esters) manufacturing process: production of 1, 3-propanediol, citric acid and single cell oil. Biomass and bioenergy, 32(1), 60-71.
Papanikolaou, S., Galiotou‐Panayotou, M., Fakas, S., Komaitis, M., & Aggelis, G. (2007). Lipid production by oleaginous Mucorales cultivated on renewable carbon sources. European Journal of Lipid Science and Technology, 109(11), 1060-1070.
Papanikolaou, S., Rontou, M., Belka, A., Athenaki, M., Gardeli, C., Mallouchos, A., ... & Aggelis, G. (2017). Conversion of biodiesel‐derived glycerol into biotechnological products of industrial significance by yeast and fungal strains. Engineering in life sciences, 17(3), 262-281.
Puiggros, C., Chacon, P., Armadans, L. I., Clapes, J., & Planas, M. (2002). Effects of oleic-rich and omega-3-rich diets on serum lipid pattern and lipid oxidation in mildly hypercholesterolemic patients. Clinical Nutrition, 21(1), 79-87.
Ratledge, C. (2004). Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie, 86(11),807-815.
Rodrigues Reis, C. E., Bento, H. B., Carvalho, A. K., Rajendran, A., Hu, B., & De Castro, H. F. (2019). Critical applications of Mucor circinelloides within a biorefinery context. Critical reviews in biotechnology, 39(4), 555-570.
Santos, R. D.A.C.M., Gagliardi H.T., Xavier, C.D, Magnoni, R., Cassani, A.M.O., Lottenberg Fenelon, G. I.. Diretriz sobre o consumo de gorduras e saúde cardiovascular. Arq. Brasileiro. Cardiologia. 2013. 100(1), 1-40.
Shah, A. M., Mohamed, H., Zhang, Z., & Song, Y. (2021). Isolation, characterization and fatty acid analysis of Gilbertella persicaria DSR1: a potential new source of high value single-cell oil. Biomass and Bioenergy, 151, 106156.
Sheehan, H. L., & Storey, G. W. (1947). An improved method of staining leucocyte granules with Sudan black B. The Journal of pathology and bacteriology, 59(1‐2), 336-337.
Sitepu, I.; Selby, T.; Lin, T.; Zhu, S.; Boundy-Mills, K. Carbon source utilization and inhibitor tolerance of 45 oleaginous yeast species. J. Ind. Microbiol. Biotechnol. 2014 , 41(7) 1061-1070.
Souza, A. F., Rodriguez, D. M., Ribeaux, D. R., Luna, M. A., Lima e Silva, T. A., Andrade, R. F. S., ... & Campos-Takaki, G. M. (2016). Waste soybean oil and corn steep liquor as economic substrates for bioemulsifier and biodiesel production by Candida lipolytica UCP 0998. International journal of molecular sciences, 17(10), 1608.
Tonato, D., Marcuz, C., Vendruscolo, R. G., Bevilacqua, C., Jacques, R. J., Wagner, R., ... & Mazutti, M. A. (2018). Production of polyunsaturated fatty acids by microorganisms isolated in the Brazilian Pampa biome. Brazilian Journal of Chemical Engineering, 35, 835-846.
Tzimorotas, D., Afseth, N. K., Lindberg, D., Kjørlaug, O., Axelsson, L., & Shapaval, V. (2018). Pretreatment of different food rest materials for bioconversion into fungal lipid-rich biomass. Bioprocess and biosystems engineering, 41(7), 1039-1049.
Ward, O. P., & Singh, A. (2005). Omega-3/6 fatty acids: alternative sources of production. Process biochemistry, 40(12), 3627-3652.
Yannakoulia, M., Mamalaki, E., Anastasiou, C. A., Mourtzi, N., Lambrinoudaki, I., & Scarmeas, N. (2018). Eating habits and behaviors of older people: Where are we now and where should we go?. Maturitas, 114, 14-21.
Zhao, L., Zhang, H., Wang, L., Chen, H., Chen, Y. Q., Chen, W., & Song, Y. (2015). 13C-metabolic flux analysis of lipid accumulation in the oleaginous fungus Mucor circinelloides. Bioresource technology, 197, 23-29.
Zininga, J. T., Puri, A. K., Govender, A., Singh, S., & Permaul, K. (2019). Concomitant production of chitosan and lipids from a newly isolated Mucor circinelloides ZSKP for biodiesel production. Bioresource technology, 272, 545-551.
Downloads
Publicado
Como Citar
Edição
Seção
Licença
Copyright (c) 2022 Adriana Ferreira de Souza; Manuela Cristina Mota Lins; Marcos Antônio Barbosa de Lima; Rosileide Fontenele da Silva Andrade; Dayana Montero Rodríguez; Norma Buarque Gusmão; Galba Maria de Campos-Takaki
Este trabalho está licenciado sob uma licença Creative Commons Attribution 4.0 International License.
Autores que publicam nesta revista concordam com os seguintes termos:
1) Autores mantém os direitos autorais e concedem à revista o direito de primeira publicação, com o trabalho simultaneamente licenciado sob a Licença Creative Commons Attribution que permite o compartilhamento do trabalho com reconhecimento da autoria e publicação inicial nesta revista.
2) Autores têm autorização para assumir contratos adicionais separadamente, para distribuição não-exclusiva da versão do trabalho publicada nesta revista (ex.: publicar em repositório institucional ou como capítulo de livro), com reconhecimento de autoria e publicação inicial nesta revista.
3) Autores têm permissão e são estimulados a publicar e distribuir seu trabalho online (ex.: em repositórios institucionais ou na sua página pessoal) a qualquer ponto antes ou durante o processo editorial, já que isso pode gerar alterações produtivas, bem como aumentar o impacto e a citação do trabalho publicado.
