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Biocatalysis and Fermentation Technology
Submerged Culture Conditions for the Production of Alternative Natural Colorants by a New Isolated Penicillium purpurogenum DPUA 1275
1Department of Biochemical and Pharmaceutical Technology, University of São Paulo, 05508-900 São Paulo, SP, Brazil, 2Culture Collection DPUA/UFAM. Universidade Federal do Amazonas, 69.077-000, Manaus, AM, Brazil
Received: November 20, 2012; Accepted: January 25, 2013
J. Microbiol. Biotechnol. 2013; 23(6): 802-810
Published June 28, 2013 https://doi.org/10.4014/jmb.1211.11057
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
This work aims at investigating the production of yellow,
orange, and red natural colorants in a submerged culture
of Penicillium purpurogenum DPUA 1275. For this purpose,
different experimental conditions evaluating the effect of
incubation time, type and size of inoculum, and different
carbon and nitrogen sources were performed. Furthermore,
the growth kinetics were obtained in the conditions of
108 spores/ml and 5 mycelia agar discs during 360 h.
These experiments showed that 5 mycelia agar discs and
336 h promoted the highest yellow (3.08 UA400nm), orange
(1.44 UA470nm), and red (2.27 UA490nm) colorants production.
Moreover, sucrose and yeast extract were the most
suitable carbon and nitrogen sources for natural colorants
production. Thus, the present study shows a new source of
natural colorants, which can be used as an alternative to
others available in the market after toxicological studies.
Keywords
natural colorants, filamentous fungi, production, submerged culture
References
- Antunes, J. G. 1997. Bioconversão de D-xilose a etanol por Pichia stipitis. [S.l.]: Universidade Federal do Rio de Janeiro.
- Babitha, S., C. R. Soccol, and A. Pandey. 2007. Solid-state fermentation for the production of Monascus pigments from jackfruit seed. Bioresource Technol. 98: 1554-1560.
- Boo, H. O., S. J. Hwang, C. S. Bae, S. H. Park, B. G. Heo, and S. Gorinstein. 2012. Extraction and characterization of some natural plant pigments. Ind. Crops Prod. 40: 129-135.
- Chen, M. H. and M. R. Johns. 1993. Effect of pH and nitrogen source on pigment production by Monascus purpureus. Appl. Microbiol. Biotechnol. 40: 132-138.
- Cho, Y. J., J. P. Park, H. J. Hwang, S. W. Kim, J. W. Choi, and J. W. Yun. 2002. Production of red pigment by submerged culture of Paecilomyces sinclairii. Lett. Appl. Microbiol. 35: 195-202.
- Deveoglu, O., E. Cakmakc , T. Taskopru, E. Torgan, and R. Karadag. 2012. Identification by RP-HPLC-DAD, FTIR, TGA and FESEM-EDAX of natural pigments prepared from Datisca cannabina. Dyes Pigments 94: 437-442.
- Dhake, A. B. and M. B. Pati. 2005. Production of β-glucosidase by Penicillium purpurogenum. Braz. J. Microbiol. 36: 170-176.
- Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. Smith. 1956. Colorimetric method for determination of sugars and related compounds. Anal. Chem. 28: 350-356.
- Dufossé, L., P. Galaup, A. Yaron, S. M. Arad, P. Blanc, K. N. C. Murthy, and G. A. Ravishankar. 2005. Microorganisms and microalgae as sources of pigments for food use: A scientific oddity or an industrial reality? Trends Food Sci. Technol. 16:389-406.
- Esposito, E. and J. L. Azevedo. 2004. Fungos: Uma introdução à biologia, bioquímica e biotecnologia. EDUCS, Caxias do Sul.
- Fang, T. J. and Y. S. Cheng. 1993. Improvement of astaxanthin production by Phaffia rhodozyma through mutation and optimization of culture conditions. J. Ferment. Bioeng. 75:466-469.
- Gams, W., R. A. Samson, and J. A. Stalpers. 1975. Course of Mycology. Academy of Sciences and Letters, England.
- Gibbs, D. H., R. J. Seviour, and F. Schmid. 2000. Growth of filamentous fungi in submerged culture: Problems and possible solutions. Crit. Rev. Biotechnol. 20: 17-48.
- Griffin, D. H. 1994. Fungal Physiology. Wiley Liss.
- Gunasekaran, S. and R. Poorniammal. 2008. Optimization of fermentation conditions for red pigment production from Penicillium sp. under submerged cultivation. Afr. J. Biotechnol. 7: 1894-1898.
- Hailei, W., R. Zhifang, L. Ping, G. Yanchang, L. Guosheng, and Y. Jianming. 2011. Improvement of the production of a red pigment in Penicillium sp. HSD07B synthesized during coculture with Candida tropicalis. Bioresource Technol. 102:6082-6087.
- Johns, M. R. and D. M. Stuart. 1991. Production of pigments by Monascus purpureus in solid culture. J. Ind. Microbiol. 8:23-38.
- Kang, S. G., J. W. Rhim, S. T. Jung, and S. J. Kim. 1996. Production of red and yellow pigment from Monascus anka in a jar fermenter. Korean J. Appl. Microbiol. Biotechnol. 24: 756762.
- Kongruang, S. 2011. Growth kinetics of biopigment production by Thai isolated Monascus purpureus in a stirred tank bioreactor. J. Ind. Microbiol. Biot. 38: 93-99.
- Lehninger, A. L. 1976. Bioquímica, Componentes Moleculares das Células, 2nd Ed. Edgard Blucher Ltda, São Paulo.
- Maldonado, M. C., A. M. S. Saad, and D. Callieri. 1989. Catabolic repression of the synthesis of inducible polygalacturonase and pectinesterase by Aspergillus níger. Curr. Microbiol. 18:303-306.
- Manachini, P. L., M. G. Fortina, and C. Partini. 1987. Purification of endopolygalacturonase produced by Rhizopus stolonifer. Biotechnol. Lett. 9: 219-224.
- Mapari, S. A. S., A. S. Meyer, U. Thrane, and J. C. Frisvad. 2009. Identification of potentially safe promising fungal cell factories for the production of polyketide natural food colorants using chematoxonomic rationale. Microb. Cell Fact. 8: 1-15.
- Mapari, S. A. S., A. S. Meyer, and U. Thrane. 2009. Photostability of natural orange-red and yellow fungal pigments in liquid food model systems. J. Agric. Food Chem. 57: 62536261.
- Mapari, S. A. S., U. Thrane, and A. S. Meyer. 2010. Fungal polyketide azaphilone pigments as future natural food colorants? Trends Biotechnol. 28: 300-307.
- Marco, H. G. and G. Gade. 2010. Biological activity of the predicted red pigment-concentrating hormone of Daphnia pulex in a crustacean and an insect. Gen. Comp. Endocrinol. 166:104-110.
- Martín, J. F., J. Casqueiro, and P. Liras. 2005. Secretion systems for secondary metabolites: How producer cells send out messages of intercellular communication. Curr. Opin. Microbiol. 8: 282293.
- Meinicke, R. M., F. Vendruscolo, D. E. Moritz, D. de Oliveira, W. Schmidell, R. W. Samohyl, and J. L. Ninow. 2012. Potential use of glycerol as substrate for the production of red pigments by Monascus ruber in submerged fermentation. Biocatal. Agric. Biotechnol. 1: 238-242.
- Méndez, A., C. Pérez, J. C. Montañéz, G. Martínez, and C. N. Aguilar. 2011. Red pigment production by Penicillium purpurogenum GH2 is influenced by pH and temperature. J. Zhejiang Univ. Sci. B 12: 961-968.
- Omura, S., H. Ikeda, A. Hanamoto, C. Takahashi, M. Shinose, Y. Takahashi, et al. 2001. Genome sequence of an industrial microorganism Streptomyces avermitilis: Deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. USA 98: 12215-12220.
- Pastrana, L., P. J. Blanc, A. L. Santerre, M. Loret, and G. Goma. 1995. Production of red pigments by Monascus ruber in synthetic media with a strictly controlled nitrogen source. Process Biochem. 30: 333-341.
- Piccoli-valle, R. H., F. J. V. Passos, I. V. Brandi, L. A. Peternelli, and D. O. Silva. 2003. Influence of different mixing and aeration regimens on pectin lyase production by Penicillium griseoroseum. Crop Sci. 38: 849-854.
- Pitt, J. 1985. A Laboratory Guide to Common Penicillium Species. CSIRO, Australia.
- Putzke, J. and M. T. L. Putzke. 2002. Reino dos Fungos. EDUNISC.
- Rapper, K. B. and D. I. Fennel. 1977. The Genus Aspergillus. Malabar Publishing Company, Florida.
- Saha, S., R. Thavasi, and S. Jayalakshmi. 2008. Phenazine pigments from Pseudomonas aeruginosa and their applications as antibacterial agent and food colourants. Res. J. Microbiol. 3:122-128.
- Samson, R. A., H. C. Evans, and J. P. Lagté. 1988. Atlas of Entomopathogenic Fungi. Springer-Verlag, Berlin, Heidelberg. New York.
- Teixeira, M. F. S., T. Amorim, R. A. Palheta, and H. M. Atayde. 2011. Fungos da Amazônia: Uma riqueza inexplorada (aplicações biotecnológicas). EDUA, Manaus.
- Teixeira, M. F. S., M. S. Martins, J. Da Silva, L. S. Kirsch, O. C. C. Fernandes, A. L. B. Carneiro, et al. 2012. Amazonian biodiversity: Pigments from Aspergillus and Penicillium characterizations, antibacterial activities and their toxicities. Curr. Trends Biotechnol. Pharmacol. 6: 300-311.
- Teng, S. S. and W. Feldheim. 2001. Anka and anka pigment production. J. Ind. Microbiol. Biotechnol. 26: 280-282.
- Unagul, P., P. Wongsa, P. Kittakoop, S. Intamas, and P. Srikitikulchai. 2005. Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis BCC 1869. J. Ind. Microbiol. Biotechnol. 32: 135-140.
- Velmurugan, P., Y. H. Lee, C. K. Venil, P. Lakshmanaperumalsamy, J. C. Chae, and B. T. Oh. 2010. Effect of light on growth, intracellular and extracellular pigment production by five pigmentproducing filamentous fungi in synthetic medium. J. Biosci. Bioeng. 109: 346-350.
- Velmurugan, P., S. Kamala-Kannan, V. Balachandar, P. Lakshmanaperumalsamy, J. C. Chae, and B. T. Oh. 2010. Natural pigment extraction from five filamentous fungi for industrial applications and dyeing of leather. Carbohydr. Polym. 79: 262268.
- Wang, L., D. Ridgway, T. Gu, and M. Moo-Young. 2005. Bioprocessing strategies to improve heterologous protein production in filamentous fungal fermentations. Biotechnol. Adv. 23: 115129.
- Wybraniec, S. 2005. Formation of decarboxylated betacyanins in heated purified fractions from red beet root (Beta vulgaris L.) monitored by LC-MS/MS. J. Agric. Food Chem. 53: 34833487.
- Yang, L. H., H. Xiong, O. O. Lee, S. H. Qi, and P. Y. Qian. 2007. Effect of agitation on violacein production in Pseudoalteromonas luteoviolacea isolated from a marine sponge. Lett. Appl. Microbiol. 44: 625-630.
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Research article
J. Microbiol. Biotechnol. 2013; 23(6): 802-810
Published online June 28, 2013 https://doi.org/10.4014/jmb.1211.11057
Copyright © The Korean Society for Microbiology and Biotechnology.
Submerged Culture Conditions for the Production of Alternative Natural Colorants by a New Isolated Penicillium purpurogenum DPUA 1275
Valeria Carvalho Santos-Ebinuma 1*, Maria Francisca Simas Teixeira 2 and Adalberto Pessoa Jr. 1
1Department of Biochemical and Pharmaceutical Technology, University of São Paulo, 05508-900 São Paulo, SP, Brazil, 2Culture Collection DPUA/UFAM. Universidade Federal do Amazonas, 69.077-000, Manaus, AM, Brazil
Received: November 20, 2012; Accepted: January 25, 2013
Abstract
This work aims at investigating the production of yellow,
orange, and red natural colorants in a submerged culture
of Penicillium purpurogenum DPUA 1275. For this purpose,
different experimental conditions evaluating the effect of
incubation time, type and size of inoculum, and different
carbon and nitrogen sources were performed. Furthermore,
the growth kinetics were obtained in the conditions of
108 spores/ml and 5 mycelia agar discs during 360 h.
These experiments showed that 5 mycelia agar discs and
336 h promoted the highest yellow (3.08 UA400nm), orange
(1.44 UA470nm), and red (2.27 UA490nm) colorants production.
Moreover, sucrose and yeast extract were the most
suitable carbon and nitrogen sources for natural colorants
production. Thus, the present study shows a new source of
natural colorants, which can be used as an alternative to
others available in the market after toxicological studies.
Keywords: natural colorants, filamentous fungi, production, submerged culture
References
- Antunes, J. G. 1997. Bioconversão de D-xilose a etanol por Pichia stipitis. [S.l.]: Universidade Federal do Rio de Janeiro.
- Babitha, S., C. R. Soccol, and A. Pandey. 2007. Solid-state fermentation for the production of Monascus pigments from jackfruit seed. Bioresource Technol. 98: 1554-1560.
- Boo, H. O., S. J. Hwang, C. S. Bae, S. H. Park, B. G. Heo, and S. Gorinstein. 2012. Extraction and characterization of some natural plant pigments. Ind. Crops Prod. 40: 129-135.
- Chen, M. H. and M. R. Johns. 1993. Effect of pH and nitrogen source on pigment production by Monascus purpureus. Appl. Microbiol. Biotechnol. 40: 132-138.
- Cho, Y. J., J. P. Park, H. J. Hwang, S. W. Kim, J. W. Choi, and J. W. Yun. 2002. Production of red pigment by submerged culture of Paecilomyces sinclairii. Lett. Appl. Microbiol. 35: 195-202.
- Deveoglu, O., E. Cakmakc , T. Taskopru, E. Torgan, and R. Karadag. 2012. Identification by RP-HPLC-DAD, FTIR, TGA and FESEM-EDAX of natural pigments prepared from Datisca cannabina. Dyes Pigments 94: 437-442.
- Dhake, A. B. and M. B. Pati. 2005. Production of β-glucosidase by Penicillium purpurogenum. Braz. J. Microbiol. 36: 170-176.
- Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. Smith. 1956. Colorimetric method for determination of sugars and related compounds. Anal. Chem. 28: 350-356.
- Dufossé, L., P. Galaup, A. Yaron, S. M. Arad, P. Blanc, K. N. C. Murthy, and G. A. Ravishankar. 2005. Microorganisms and microalgae as sources of pigments for food use: A scientific oddity or an industrial reality? Trends Food Sci. Technol. 16:389-406.
- Esposito, E. and J. L. Azevedo. 2004. Fungos: Uma introdução à biologia, bioquímica e biotecnologia. EDUCS, Caxias do Sul.
- Fang, T. J. and Y. S. Cheng. 1993. Improvement of astaxanthin production by Phaffia rhodozyma through mutation and optimization of culture conditions. J. Ferment. Bioeng. 75:466-469.
- Gams, W., R. A. Samson, and J. A. Stalpers. 1975. Course of Mycology. Academy of Sciences and Letters, England.
- Gibbs, D. H., R. J. Seviour, and F. Schmid. 2000. Growth of filamentous fungi in submerged culture: Problems and possible solutions. Crit. Rev. Biotechnol. 20: 17-48.
- Griffin, D. H. 1994. Fungal Physiology. Wiley Liss.
- Gunasekaran, S. and R. Poorniammal. 2008. Optimization of fermentation conditions for red pigment production from Penicillium sp. under submerged cultivation. Afr. J. Biotechnol. 7: 1894-1898.
- Hailei, W., R. Zhifang, L. Ping, G. Yanchang, L. Guosheng, and Y. Jianming. 2011. Improvement of the production of a red pigment in Penicillium sp. HSD07B synthesized during coculture with Candida tropicalis. Bioresource Technol. 102:6082-6087.
- Johns, M. R. and D. M. Stuart. 1991. Production of pigments by Monascus purpureus in solid culture. J. Ind. Microbiol. 8:23-38.
- Kang, S. G., J. W. Rhim, S. T. Jung, and S. J. Kim. 1996. Production of red and yellow pigment from Monascus anka in a jar fermenter. Korean J. Appl. Microbiol. Biotechnol. 24: 756762.
- Kongruang, S. 2011. Growth kinetics of biopigment production by Thai isolated Monascus purpureus in a stirred tank bioreactor. J. Ind. Microbiol. Biot. 38: 93-99.
- Lehninger, A. L. 1976. Bioquímica, Componentes Moleculares das Células, 2nd Ed. Edgard Blucher Ltda, São Paulo.
- Maldonado, M. C., A. M. S. Saad, and D. Callieri. 1989. Catabolic repression of the synthesis of inducible polygalacturonase and pectinesterase by Aspergillus níger. Curr. Microbiol. 18:303-306.
- Manachini, P. L., M. G. Fortina, and C. Partini. 1987. Purification of endopolygalacturonase produced by Rhizopus stolonifer. Biotechnol. Lett. 9: 219-224.
- Mapari, S. A. S., A. S. Meyer, U. Thrane, and J. C. Frisvad. 2009. Identification of potentially safe promising fungal cell factories for the production of polyketide natural food colorants using chematoxonomic rationale. Microb. Cell Fact. 8: 1-15.
- Mapari, S. A. S., A. S. Meyer, and U. Thrane. 2009. Photostability of natural orange-red and yellow fungal pigments in liquid food model systems. J. Agric. Food Chem. 57: 62536261.
- Mapari, S. A. S., U. Thrane, and A. S. Meyer. 2010. Fungal polyketide azaphilone pigments as future natural food colorants? Trends Biotechnol. 28: 300-307.
- Marco, H. G. and G. Gade. 2010. Biological activity of the predicted red pigment-concentrating hormone of Daphnia pulex in a crustacean and an insect. Gen. Comp. Endocrinol. 166:104-110.
- Martín, J. F., J. Casqueiro, and P. Liras. 2005. Secretion systems for secondary metabolites: How producer cells send out messages of intercellular communication. Curr. Opin. Microbiol. 8: 282293.
- Meinicke, R. M., F. Vendruscolo, D. E. Moritz, D. de Oliveira, W. Schmidell, R. W. Samohyl, and J. L. Ninow. 2012. Potential use of glycerol as substrate for the production of red pigments by Monascus ruber in submerged fermentation. Biocatal. Agric. Biotechnol. 1: 238-242.
- Méndez, A., C. Pérez, J. C. Montañéz, G. Martínez, and C. N. Aguilar. 2011. Red pigment production by Penicillium purpurogenum GH2 is influenced by pH and temperature. J. Zhejiang Univ. Sci. B 12: 961-968.
- Omura, S., H. Ikeda, A. Hanamoto, C. Takahashi, M. Shinose, Y. Takahashi, et al. 2001. Genome sequence of an industrial microorganism Streptomyces avermitilis: Deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. USA 98: 12215-12220.
- Pastrana, L., P. J. Blanc, A. L. Santerre, M. Loret, and G. Goma. 1995. Production of red pigments by Monascus ruber in synthetic media with a strictly controlled nitrogen source. Process Biochem. 30: 333-341.
- Piccoli-valle, R. H., F. J. V. Passos, I. V. Brandi, L. A. Peternelli, and D. O. Silva. 2003. Influence of different mixing and aeration regimens on pectin lyase production by Penicillium griseoroseum. Crop Sci. 38: 849-854.
- Pitt, J. 1985. A Laboratory Guide to Common Penicillium Species. CSIRO, Australia.
- Putzke, J. and M. T. L. Putzke. 2002. Reino dos Fungos. EDUNISC.
- Rapper, K. B. and D. I. Fennel. 1977. The Genus Aspergillus. Malabar Publishing Company, Florida.
- Saha, S., R. Thavasi, and S. Jayalakshmi. 2008. Phenazine pigments from Pseudomonas aeruginosa and their applications as antibacterial agent and food colourants. Res. J. Microbiol. 3:122-128.
- Samson, R. A., H. C. Evans, and J. P. Lagté. 1988. Atlas of Entomopathogenic Fungi. Springer-Verlag, Berlin, Heidelberg. New York.
- Teixeira, M. F. S., T. Amorim, R. A. Palheta, and H. M. Atayde. 2011. Fungos da Amazônia: Uma riqueza inexplorada (aplicações biotecnológicas). EDUA, Manaus.
- Teixeira, M. F. S., M. S. Martins, J. Da Silva, L. S. Kirsch, O. C. C. Fernandes, A. L. B. Carneiro, et al. 2012. Amazonian biodiversity: Pigments from Aspergillus and Penicillium characterizations, antibacterial activities and their toxicities. Curr. Trends Biotechnol. Pharmacol. 6: 300-311.
- Teng, S. S. and W. Feldheim. 2001. Anka and anka pigment production. J. Ind. Microbiol. Biotechnol. 26: 280-282.
- Unagul, P., P. Wongsa, P. Kittakoop, S. Intamas, and P. Srikitikulchai. 2005. Production of red pigments by the insect pathogenic fungus Cordyceps unilateralis BCC 1869. J. Ind. Microbiol. Biotechnol. 32: 135-140.
- Velmurugan, P., Y. H. Lee, C. K. Venil, P. Lakshmanaperumalsamy, J. C. Chae, and B. T. Oh. 2010. Effect of light on growth, intracellular and extracellular pigment production by five pigmentproducing filamentous fungi in synthetic medium. J. Biosci. Bioeng. 109: 346-350.
- Velmurugan, P., S. Kamala-Kannan, V. Balachandar, P. Lakshmanaperumalsamy, J. C. Chae, and B. T. Oh. 2010. Natural pigment extraction from five filamentous fungi for industrial applications and dyeing of leather. Carbohydr. Polym. 79: 262268.
- Wang, L., D. Ridgway, T. Gu, and M. Moo-Young. 2005. Bioprocessing strategies to improve heterologous protein production in filamentous fungal fermentations. Biotechnol. Adv. 23: 115129.
- Wybraniec, S. 2005. Formation of decarboxylated betacyanins in heated purified fractions from red beet root (Beta vulgaris L.) monitored by LC-MS/MS. J. Agric. Food Chem. 53: 34833487.
- Yang, L. H., H. Xiong, O. O. Lee, S. H. Qi, and P. Y. Qian. 2007. Effect of agitation on violacein production in Pseudoalteromonas luteoviolacea isolated from a marine sponge. Lett. Appl. Microbiol. 44: 625-630.
