Optimization of pigment production by Rhodotorula minuta URM 5197 and Rhodotorula mucilaginosa URM 7409 using yellow passion fruit peel (Passiflora edulis)

Authors

DOI:

https://doi.org/10.33448/rsd-v10i17.24311

Keywords:

Bioprocesses; Carotenoids; Agro-industrial Waste; Response surface.

Abstract

The objective of this work was to optimize the production of pigments by Rhodotorula minuta and Rhodotorula mucilaginosa through submerged fermentation, using yellow passion fruit peel (Passiflora edulis), as the only substrate. The independent variables evaluated to optimize were: yellow passion fruit peel (YPFP), in grams (g) as culture medium, pH and fermentation time, in days. The study of pigment production and its optimization was carried out using the Doehlert matrix, with fifteen experimental conditions, of which thirteen had different combinations and two repeated the central point. The fixed variables were 30ºC and 150 rpm. Data analysis was performed using the Statistica software version 10.0. The largest amount of total pigments and total carotenoids produced by R. minuta was 28±0.01 mg/L and 72.8±0.026 µg/g, respectively; while for R. mucilaginosa the production of total pigments was 37±0.002 mg/L and total carotenoids 236.8±0.013 µg/g. The optimum production point of total pigments for R. minuta was 2.3g of YPFP, pH 6.5 and 5 days and for R. mucilaginosa 2.5g of YPFP pH 6 and 5 days. In samples of total pigments, the presence of 0.29mg/L of β-carotene for R. minuta and 0.83 mg/L for R. mucilaginosa was identified. It is possible to conclude that yellow passion fruit peel can be used as a nutrient source for Rhodotorula spp growth and pigment production with total carotenoids and β-carotene in its composition.

Author Biographies

Thamilly Moreira Silva, State University of Southwest Bahia

Graduada em Nutrição, Especialista (Latu-sensu) em Nutrição Clínica e Saúde Pública, Doutoranda em Bioquímica e Biologia Molecular.

Abdias Batista da Silva Neto, University of Santa Cruz

Graduado em Ciências Biológicas e Mestrando em Biologia e Biotecnologia de Microrganismos.

Jabson Meneses Teixeira, University of Santa Cruz

Graduado em Ciências Biológicas e Mestrando em Biologia e Biotecnologia de Microrganismos.

Carlos Bernard Moreno Cerqueira-Silva, State University of Southwest Bahia

Graduado em Ciências Biológicas, Especialista (Latu-sensu) em Genética, Mestre e Doutor em Genética e Biologia Molecular. Professor Adjunto da Universidade Estadual do Sudoeste da Bahia (UESB). 

Simone Andrade Gualberto, State University of Southwest Bahia

Graduada em Farmácia, Especialização (Latu-sensu) em Desenho de Fármacos, Doutorado em Ciências Farmacêuticas, Pós-doutorado em Química de Produtos Naturais na Universidad de Salamanca (USAL) -  Salamanca - Espanha. Professora Pleno da Universidade Estadual do Sudoeste da Bahia (UESB).

Janaína Silva de Freitas, State University of Southwest Bahia

Graduada (Licenciada e Bacharel) em Ciências Biológicas, Doutora em Bioquímica. Professora Titular da Universidade Estadual do Sudoeste da Bahia (UESB). 

References

Aruldas, C. A., Dufossé, L. & Ahmad, W. A. (2018). Current perspective of yellowish – Orange pigments from microorganisms – a review. Journal of Cleaner Production. 180, 168-182. 10.1016/j.jclepro.2018.01.093.

Association of Official Analytical Chemists – AOAC (2016). Official Methods of Analysis of AOAC International.20 th ed. Rockville, Maryland: AOAC International.

Buzzini, P. & Martini, A. (2000). Production of carotenoids by strains of Rhodotorula glutinis cultured in raw materials of agro-industrial origin. Bioresource Technology, 71, 41- 44. 10.1016/S0960-8524(99)00056-5.

Caddick, M. X., Brownlee, A. G. & Arst, H. N. Jr (1986). Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Molecular and General Genetics. 203, 346-353.

Cavalcante, T. Q. & Melo, M. de O. (2019). Utilização de biomassa de maracujá-amarelo (Passiflora edulis f. flavicarpa) in natura como bioadsorvente para remoção de íons de Cd e Pb em meio aquoso. In: XXIII Seminário de Iniciação Científica da UEFS. Semana Nacional de Científica e Tecnológica - 2019, 23. 10.13102/semic.v0i23.6380.

Cheng, Y-T. & Yang, C-F. (2016). Using strain Rhodotorula mucilaginosa to produce carotenoids using food wastes. Journal of the Taiwan Institute of Chemical Engineers. 61, 270 - 275. 10.1016/j.jtice.2015.12.027.

Davies, B. H. (1976). Chemical Biochemistry Plant Pigments. Academic press, New York, USA.

Delgado-Vargas, F. & Peredes-López, O. (2002). Natural Colorants for Food and Nutraceutical Uses, CRC Press: Boca Raton, FL, USA, 1-344.

Freitas, J. S, Silva, E. M. & Rossi, A. (2007). Identification of nutrient-dependent changes in extracellular pH and acid phosphatase secretion in Aspergillus nidulans. Genetics and Molecular Research. 6 (3), 721-729.

Gerelmaa, Z., Zultsetseg, Ch., Batjargal B. & Rentsenkhand, Ts. (2018). Selection of culture media for the production of carotenoids with antioxidant activity by Rhodotorula glutinis. Proceedings of the Mongolian Academy of Sciences. 58 (4), 31-38. 10.5564/pmas.v58i4.1047.

Gómez-Garcia, M. R. & Ochoa-Alejo, N. (2013). Biochemistry and molecular biology of carotenoid biosynthesis in chili peppers (Capsicum spp.). International Journal of Molecular Sciences, 14 (9), 19025 - 19053. 10.3390/ijms140919025.

Guzman, I., Hamby, S., Romero, J., Bosland, P. W. & O’Connell, M. (2010). Variability of carotenoid biosynthesis in Orange colored Capsicum spp. Plant Science. 179 (1-2), 49 - 59. 10.1016/j.plantsci.2010.04.014.

Heer, K. & Sharma, S. (2017). Microbial pigments as a natural color: A Review. International Journal of Pharmaceutical Sciences and Research, 8 (5), 1913-1922.

Kot, A. M., Blazejak, S., Kieliszek, M., Gientka, I., Piwowarek, K. & Brzezińska, R. (2020). Production of lipids and carotenoids by Rhodotorula gracilis ATCC 10788 yeast in a bioreactor using low - cost wastes. Biocatalysis and Agricultural Biotechnology, 26, 1-8. 10.1016/j.bcab.2020.101634.

Kot, A. M., Blazejak, S. & Kurez, A. (2016). Rhodotorula glutinis – potential source of lipids, carotenoids, and enzymes for use in industries. Applied Microbiology and Biotechnology, 100 (14), 6103-6117. 10.1007/s00253-016-7611-8.

Maccheroni., W. Jr., Pombeiro, S. R. C., Martinez-Rossi, N. M. & Rossi, A. (1991). pH and acid phosphatase determinations after growth of Aspergillus nidulans on solid medium. Fungal Genetics Reports, 38 (8), 78-79. 10.4148/1941-4765.1454.

Machado, W. R. C., Soares, B. V. & Del Bianchi, V. L. (2019). Produção de carotenoides por meio de fermentação em estado sólido com Rhodotorula mucilaginosa em bagaço de laranja (Citrus sinensis). Revista de Engenharia e Tecnologia, 11(3), 48-57.

Malisorn, C. & Suntornsuk, W. (2008). Optimization of β-carotene production by Rhodotorula glutinis DM28 in fermented radish brine. Bioresource Technology, 99 (7), 2281 - 2287.10.1016/j.biortech.2007.05.019.

Manimala, M. R. A & Murugesan, R. (2017). Carotenoid pigment production from Yeast: Health benefits and their industrial applications. International Journal of Chemistry, 5, 392-395.

Manimala, M. R. A. & Murugusan, R. (2018). Characterization of carotenoid pigment production from yeast Sporobolomyces sp. and their application in food products. Journal of Phamacognosy and Phytochemistry. 7 (1), 2818-2821.

Mata-Gómez, L. C., Montañez, J. C., Méndez-Zavala, A. & Aguilar, C. N. (2014). Biotechnological production of carotenoids by yeasts: an overview. Microbial Cell Factories. 13 (12), 2-11.

Menezes, J. D. S., Druzian, J. I., Padilha, F. F. & Souza, R. R. (2012). Produção Biotecnológica de goma xantana em alguns resíduos agroindustriais, caracterização e aplicações. Revista Eletrônica em Gestão, Educação e Tecnologia Ambiental, 8 (8),1761-1776.

Moliné, M., Libkind, D. & Van Broock, M. (2012). Production of torularhodin, torulene and β-carotene by Rhodotorula yeasts. Methods in Molecular Biology, 898, 275 - 283. 10.1007/978-1-61779-918-1_19.

Moriel, D. G., Chociai, M. B., Machado, I. M. P., Fontana, J. D. & Bonfim, T. M. B. (2005). Effect of feeding methods on the astaxanthin production by Phaffia rhodozyma in fed-batch process. Brazilian Archives of Biology and Technology, 48, 397- 401. 10.1590/S151689132005000300010.

Mussagy, C. U., Winterburn, J., Santos-Ebinuma, V. C. & Pereira, J. F. B. (2018). Production and extraction of carotenoids produced by microorganisms. Applied Microbiology and Biotechnology,103, 1095-1114. 10.1007/s00253-018-9557-5.

Nabi, F., Arain, M. A., Rajput, N., Alagawany, M., Soomro, J., Umer, M., Soomro, F., Wang, Z., Ye, R. & Liu, J. (2020). Health benefits of carotenoids and potential application in poultry industry: A review. Journal of Animal Physiology and Animal Nutrition, 104, 1809-1818. /10.1111/jpn.13375.

Nahas, E., Terenzi, H. F. & Rossi, A. (1982). Effect of carbon source and pH on the production and secretion of acid phosphatase (EC 3.1.3.2) and alkaline phosphatase (EC 3.1.3.1) in Neurospora crassa. Journal of General Microbiology. 128, 2017-2021. 10.1099/00221287-128-9-2017.

Peñalva, M. A. & Arst, H. N. Jr (2004). Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annual Review of Microbiology. 58, 425-451. 10.1146/annurev.micro.58.030603.123715.

Panesar, R., Kaur, S. & Panesar, P. S. (2015). Production of microbial pigments utilizing agro-industrial waste: a review. Current Opinion in Food Science, 1, 70-76. 10.1016/j.cofs.2014.12.002.

Petrik, S., Marova, I., Haronikova, A., Kostovova, I. & Breierova, E. (2013). Production of biomass, carotenoid and other lipid metabolites by several red yeast strains cultivated on waste glycerol from biofuel production - a comparative screening study. Annals of Microbiology, 63, 1537-1551. 10.1007/s13213-013-0617-x

Rodrigues, T. A., Schueler, T. A., da Silva, J. R., Sérvulo, E. F. C. & Oliveira, F. J. S. (2019). Valorization of solid wastes from the brewery and biodiesel industries for the bioproduction of natural dye. Brazilian Journal of Chemical Engineering, 36 (1), 99 -107. 10.1590/0104-6632.20190361s20170608.

Sen, T., Barrow, C. J. & Deshmukh, S. K. (2019). Microbial Pigments in the Food Industry - Challenges and the Way Forward. Frontiers in Nutrition, 6 (7), 1-14. 10.3389/fnut.2019.00007.

Silva, J. da, Silva, F. L. H. da, Ribeiro, E. S., Melo, D. J. N. de, Santos, F. A. & Medeiros, L. L. de. (2020). Effect of supplementation, temperature and pH on carotenoids and lipids production by Rhodotorula mucilaginosa on sisal bagasse hydrolyzate. Biocatalysis and Agricultural Biotechnology, 30, 1-7.

Silva, S. R. S., Stamford, T. C. M., Albuquerque, W. W. C., Vidal, E. E. & Stamford, T. L. M. (2020). Reutilization of residual glycerin for the produce b-carotene by Rhodotorula minuta. Biotechnology Letters, 42, 437- 443.

Squina, F. M., Yamashita, F., Pereira, J. L. & Mercadante, A. Z. (2002). Production of carotenoids by Rhodotorula rubra and R. glutinis in culture medium supplemented with sugar cane juice. Food Biotechnology, 16 (3), 227 - 235. 10.1081/FBT-120016776.

Sola, M. C, Oliveira, A. P., Feistel, J. C. & Rezende, C. S. M. (2012). Manutenção de microrganismos: Conservação e Viabilidade. Enciclopédia Biosfera. Centro Científico Conhecer, 8 (14), 1398 - 1418.

Taskin, M., Sisman, T., Erdal, S. & Kurbanoglu, E. B. (2011). Use of waste chicken feathers as peptone for production of carotenoids in submerged culture of Rhodotorula glutinis MT-5. European Food Research and Technology, 223, 657 - 665.

Tinoi, J., Rakariyatham, N. & Deming, R. L. (2005). Simplex optimization of carotenoid production by Rhodotorula glutinis using hydrolysed mung bean waste flour as substrate. Process Biochemistry, 40 (7), 2551 - 2557.

Van Soest, P. J., Robertson, J. B. & Lewis, B. A. (1991). Methods for Dietary Fiber, Neutral Detergent Fiber, and Nonstarch Polysaccharides in Relation to Animal Nutrition. Journal of Dairy Science, 74 (10), 3583-3597.

Venil, C. K, Zakaria, Z. A. & Ahmad, W. A. (2013). Bacterial pigments and their applications. Process Biochemistry, 48 (7), 1065-1079. 10.1016/j.procbio.2013.06.006.

Viana, L. G. & Cruz, P. S. (2016). Reaproveitamento de Resíduos Agroindustriais. In: Congresso Baiano de Engenharia Sanitária e Ambiental, IV COBESA. 1-3.

Weedon, B. C. L. & Moss, G. P. (1995). Structure and Nomenclature. In Carotenoids; Britton, G., Liaaen-Jensen, S., Pfander, H. P., Eds.; Birkhäuser Verlag: Basel, Switzerland, I B: Spectroscopy, 27-70.

Yadav, K. S. & Prabha, R. (2014). Extraction of Pigments from Rhodotorula Species of Dairy Environment. Indian Journal of Science and Technology, 7 (12),1973-1977. 10.17485/ijst/2014/v7i12.28.

Downloads

Published

22/12/2021

How to Cite

SILVA, T. M. .; SILVA NETO, A. B. da .; TEIXEIRA, J. M. .; CERQUEIRA-SILVA, C. B. M. .; GUALBERTO, S. A.; FREITAS, J. S. de . Optimization of pigment production by Rhodotorula minuta URM 5197 and Rhodotorula mucilaginosa URM 7409 using yellow passion fruit peel (Passiflora edulis). Research, Society and Development, [S. l.], v. 10, n. 17, p. e152101724311, 2021. DOI: 10.33448/rsd-v10i17.24311. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/24311. Acesso em: 17 jan. 2022.

Issue

Section

Agrarian and Biological Sciences