Perstraction of Intracellular Pigments through Submerged Fermentation of Talaromyces spp. in a Surfactant Rich Media: A Novel Approach for Enhanced Pigment Recovery
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microorganism
2.2. Culture Media
2.3. Inoculum Preparation
2.4. Cultivation Conditions
2.5. Analytical Methods
2.6. Cloud Point Extraction
2.7. Kinetic Parameters
2.8. Data Analysis
3. Results and Discussion
3.1. Effect of Surfactants on Secretion of Intracellular Pigments into Fermentation Broth (Screening)
3.2. Effect of Addition Time of Triton X-100 during the Fermentation
3.3. Pigments Production Kinetics of Talaromyces spp. by Using Triton X-100
3.4. Pigments Partitioning in Cloud Point System
4. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Grunert, K.G. Food quality and safety: Consumer perception and demand. Eur. Rev. Agric. Econ. 2005, 32, 369–391. [Google Scholar] [CrossRef]
- El-Wahab, H.M.; Moram, G.S. Toxic effects of some synthetic food colorants and/or flavor additives on male rats. Toxicol. Ind. Health 2013, 29, 224–232. [Google Scholar] [CrossRef] [PubMed]
- Carocho, M.; Barreiro, M.F.; Morales, P.; Ferreira, I.C. Adding molecules to food, pros and cons: A review on synthetic and natural food additives. Compr. Rev. Food Sci. Food Saf. 2014, 13, 377–399. [Google Scholar] [CrossRef]
- Onslow, M.W. The Anthocyanin Pigments of Plants; Cambridge University Press: Cambridge, UK, 2014. [Google Scholar]
- Boo, H.O.; Hwang, S.J.; Bae, C.S.; Park, S.H.; Heo, B.G.; Gorinstein, S. Extraction and characterization of some natural plant pigments. Ind. Crop. Prod. 2012, 40, 129–135. [Google Scholar] [CrossRef]
- Borges, M.E.; Tejera, R.L.; Díaz, L.; Esparza, P.; Ibáñez, E. Natural dyes extraction from cochineal (Dactylopius coccus). New extraction methods. Food Chem. 2012, 132, 1855–1860. [Google Scholar] [CrossRef]
- Tuli, H.S.; Chaudhary, P.; Beniwal, V.; Sharma, A.K. Microbial pigments as natural color sources: Current trends and future perspectives. J. Food Sci. Technol. 2015, 52, 4669–4678. [Google Scholar] [CrossRef] [PubMed]
- Dufosse, L.; Fouillaud, M.; Caro, Y.; Mapari, S.A.; Sutthiwong, N. Filamentous fungi are large-scale producers of pigments and colorants for the food industry. Curr. Opin. Biotechnol. 2014, 26, 56–61. [Google Scholar] [CrossRef] [PubMed]
- Feng, Y.; Shao, Y.; Chen, F. Monascus pigments. Appl. Microbiol. Biotechnol. 2012, 96, 1421–1440. [Google Scholar] [CrossRef] [PubMed]
- Hajjaj, H.; Blanc, P.; Groussac, E. Kinetic analysis of red pigment and citrinin production by Monascus ruber as a function of organic acid accumulation. Enzym. Microb. Technol. 2000, 27, 619–625. [Google Scholar] [CrossRef]
- Morales-Oyervides, L.; Oliveira, J.C.; Sousa-Gallagher, M.J.; Méndez-Zavala, A.; Montañez, J.C. Selection of best conditions of inoculum preparation for optimum performance of the pigment production process by Talaromyces spp. using the Taguchi method. Biotechnol. Prog. 2017. [Google Scholar] [CrossRef] [PubMed]
- Santos-Ebinuma, V.C.; Roberto, I.C.; Simas Teixeira, M.F.; Pessoa, A. Improving of red colorants production by a new Penicillium purpurogenum strain in submerged culture and the effect of different parameters in their stability. Biotechnol. Prog. 2013, 29, 778–785. [Google Scholar] [CrossRef] [PubMed]
- Morales-Oyervides, L.; Oliveira, J.C.; Sousa-Gallagher, M.J.; Méndez-Zavala, A.; Montañez, J.C. Effect of heat exposure on the colour intensity of red pigments produced by Penicillium purpurogenum GH2. J. Food Eng. 2015, 164, 21–29. [Google Scholar] [CrossRef]
- Dhale, M.A.; Vijay-Raj, A.S. Pigment and amylase production in Penicillium sp NIOM-02 and its radical scavenging activity. Int. J. Food Sci. Technol. 2009, 44, 2424–2430. [Google Scholar] [CrossRef]
- Teixeira, M.; Teixeira, M.F.; Martins, M.; Caldas, J.; Kirsh, L.; Fernandes, O.; Fernandes, O.C.; Carneiro, A.; De Conti, R.; Durán, N. Amazonian biodiversity: Pigments from Aspergillus and Penicillium-characterizations, antibacterial activities and their toxicities. Curr. Trends Biotechnol. Pharm. 2012, 6, 300–311. [Google Scholar]
- Sopandi, T.; Wardah, W. Sub-Acute toxicity of pigment derived from Penicillium resticulosum in mice. Microbiol. Indones. 2012, 6, 35–41. [Google Scholar] [CrossRef]
- Ziolkowska, J.R.; Simon, L. Recent developments and prospects for algae-based fuels in the US. Renew. Sustain. Energy Rev. 2014, 29, 847–853. [Google Scholar] [CrossRef]
- Glembin, P.; Kerner, M.; Smirnova, I. Cloud point extraction of microalgae cultures. Sep. Purif. Technol. 2013, 103, 21–27. [Google Scholar] [CrossRef]
- Qureshi, N.; Maddox, I.S. Reduction in butanol inhibition by perstraction, utilization of concentrated Lactose/Whey permeate by Clostridium acetobutylicum to enhance butanol fermentation Economics. Food Bioprod. Process. 2005, 83, 43–52. [Google Scholar] [CrossRef]
- Hu, Z.; Zhang, X.; Wu, Z.; Qi, H.; Wang, Z. Perstraction of intracellular pigments by submerged cultivation of Monascus in nonionic surfactant micelle aqueous solution. Appl. Microbiol. Biotechnol. 2012, 94, 81–89. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Wang, Y.-L.; Lu, L.-P.; Zhang, B.-B.; Xu, G.-R. Enhanced production of Monacolin K by addition of precursors and surfactants in submerged fermentation of Monascus purpureus 9901. Biotechnol. Appl. Biochem. 2014, 61, 202–207. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Zhang, B.; Lu, L.; Huang, Y.; Xu, G. Enhanced production of pigments by addition of surfactants in submerged fermentation of Monascus purpureus H1102. J. Sci. Food Agric. 2013, 93, 3339–3344. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z. The potential of cloud point system as a novel two-phase partitioning system for biotransformation. Appl. Microbiol. Biotechnol. 2007, 75, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Pan, T.; Wang, Z.; Xu, J.H.; Wu, Z.; Qi, H. Extractive fermentation in cloud point system for lipase production by Serratia marcescens ECU1010. Appl. Microbiol. Biotechnol. 2010, 85, 1789–1796. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Wang, Z.; Li, W.; Zhuang, B.; Qi, H. Production of l-phenylacetylcarbinol by microbial transformation in polyethylene glycol-induced cloud point system. Appl. Microbiol. Biotechnol. 2008, 78, 233–239. [Google Scholar] [CrossRef] [PubMed]
- Kang, B.; Zhang, X.; Wu, Z.; Qi, H.; Wang, Z. Effect of pH and nonionic surfactant on profile of intracellular and extracellular Monascus pigments. Process Biochem. 2013, 48, 759–767. [Google Scholar] [CrossRef]
- Cruz-Hernández, M; Rodráguez, R. Aislamiento y caracterización morfológica de cepas microbianas degradadotas de taninos. In Proceedings of the XXII Annual Meeting of the Mexican Academy of Chemical Engineering (AMIDIQ), Mazatlan, Mexico, 9 September 2001; pp. 71–72. [Google Scholar]
- Espinoza-Hernández, T. Caracterización Morfológica, Fisiológica y Molecular de Tres Cepas Fúngicas Productoras de Pigmentos. Bachelor’s Thesis, Universidad Autónoma de Coahuila, Saltillo, Mexico, 2004. [Google Scholar]
- Frisvad, J.C.; Yilmaz, N.; Thrane, U.; Rasmussen, K.B.; Houbraken, J.; Samson, R.A. Talaromyces atroroseus, a new species efficiently producing industrially relevant red pigments. PLoS ONE 2013, 8, e84102. [Google Scholar] [CrossRef] [PubMed]
- Méndez-Zavala, A. Identificación de Factores que Afectan la Producción de Pigmentos por Penicillium purpurogenum GH2 y Obtención de Perfiles Cromatográficos. Master’s Thesis, Universidad Autónoma de Coahuila, Saltillo, Mexico, 2011. [Google Scholar]
- Morales-Oyervides, L.; Oliveira, J.C.; Sousa-Gallagher, M.J.; Méndez-Zavala, A.; Montañez, J.C. Quantitative assessment of the impact of the type of inoculum on the kinetics of cell growth, substrate consumption and pigment productivity by Penicillium purpurogenum GH2 in liquid culture with an integrated stochastic approach. Food Bioprod. Process. 2015, 96, 221–231. [Google Scholar] [CrossRef]
- Méndez-Zavala, A.; Pérez, C.; Montañez, J.C.; Martínez, G.; Aguilar, C.N. Red pigment production by Penicillium purpurogenum GH2 is influenced by pH and temperature. J. Zhejiang Univ. Sci. B 2011, 12, 961–968. [Google Scholar] [CrossRef] [PubMed]
- Dubois, M.; Gilles, K.; Hamilton, J. Colorimetric method for determination of sugars and related substances. Anal. Chem. 1956, 28, 300–306. [Google Scholar] [CrossRef]
- Kang, B.; Zhang, X.; Wu, Z.; Qi, H.; Wang, Z. Isolation of natural red colorants from fermented broth using ionic liquid-based aqueous two-phase systems. J. Ind. Microbiol. Biotechnol. 2013, 40, 507–516. [Google Scholar]
- Babitha, S.; Soccol, C.R.; Pandey, A. Effect of stress on growth, pigment production and morphology of Monascus sp. in solid cultures. J. Basic Microbiol. 2007, 47, 118–126. [Google Scholar] [CrossRef]
- Velmurugan, P. Studies on the Production and Dyeing Properties of Water Soluble Pigments from Filamentous Fungi. Ph.D. Thesis, Bharathiar University, Coimbatore, India, 2008. [Google Scholar]
- Dafoe-Samper, T. Properties of Absorbent Polymer Extractants for the Selective Removal of Target Molecules from Fermentation Systems. Ph.D. Thesis, Queen’s University, Kingston, ON, Canada, 2014. [Google Scholar]
- Kim, S.W.; Seo, W.T.; Park, Y.H. Enhanced production of β-carotene from Blakeslea trispora with Span 20. Biotechnol. Lett. 1997, 19, 557–560. [Google Scholar] [CrossRef]
- Zhang, H.; Xia, Y.J.; Wang, Y.L.; Zhang, B.B.; Xu, G.R. Coupling use of surfactant and in situ extractant for enhanced production of Antrodin C by submerged fermentation of Antrodia camphorata. Biochem. Eng. J. 2013, 79, 194–199. [Google Scholar] [CrossRef]
- Hu, Z.; Zhang, X.; Wu, Z.; Qi, H.; Wang, Z. Export of intracellular Monascus pigments by two-stage microbial fermentation in nonionic surfactant micelle aqueous solution. J. Biotechnol. 2012, 162, 202–209. [Google Scholar] [CrossRef] [PubMed]
- Dhamole, P.B.; Wang, Z.; Liu, Y.; Wang, B.; Feng, H. Extractive fermentation with non-ionic surfactants to enhance butanol production. Biomass Bioenergy 2012, 40, 112–119. [Google Scholar] [CrossRef]
- Deive, F.J.; Carvalho, E.; Pastrana, L.; Rúa, M.L.; Longo, M.A.; Sanroman, M.A. Strategies for improving extracellular lipolytic enzyme production by Thermus thermophilus HB27. Bioresour. Technol. 2009, 100, 3630–3637. [Google Scholar] [CrossRef] [PubMed]
- Mavituna, F.; Sinclair, C. Practical Fermentation Technology; John Wiley & Sons: West Sussex, UK, 2008; p. 402. [Google Scholar]
- Van Bodegom, P. Microbial maintenance: A critical review on its quantification. Microb. Ecol. 2007, 53, 513–523. [Google Scholar] [CrossRef] [PubMed]
- Patil, S.; Sivanandhan, G.; Thakare, D. Effect of physical and chemical parameters on the production of Red exopigment from Penicillium purpurogenum isolated from spoilt onion and study of its antimicrobial activity. Int. J. Curr. Microbiol. Appl. Sci. 2015, 4, 599–609. [Google Scholar]
Kinetics | Rate, k | Ratio | |
---|---|---|---|
Intracellular, OD500/h | Biomass, g/L/h | KI/KB, OD500, L/g | |
A | −0.023 ± 0.001 | −0.0125 ± 0.002 | 1.90 ± 0.19 |
B | −0.103 ± 0.004 | −0.052 ± 0.004 | 1.97 ± 0.10 |
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Morales-Oyervides, L.; Oliveira, J.; Sousa-Gallagher, M.; Méndez-Zavala, A.; Montañez, J.C. Perstraction of Intracellular Pigments through Submerged Fermentation of Talaromyces spp. in a Surfactant Rich Media: A Novel Approach for Enhanced Pigment Recovery. J. Fungi 2017, 3, 33. https://doi.org/10.3390/jof3030033
Morales-Oyervides L, Oliveira J, Sousa-Gallagher M, Méndez-Zavala A, Montañez JC. Perstraction of Intracellular Pigments through Submerged Fermentation of Talaromyces spp. in a Surfactant Rich Media: A Novel Approach for Enhanced Pigment Recovery. Journal of Fungi. 2017; 3(3):33. https://doi.org/10.3390/jof3030033
Chicago/Turabian StyleMorales-Oyervides, Lourdes, Jorge Oliveira, Maria Sousa-Gallagher, Alejandro Méndez-Zavala, and Julio Cesar Montañez. 2017. "Perstraction of Intracellular Pigments through Submerged Fermentation of Talaromyces spp. in a Surfactant Rich Media: A Novel Approach for Enhanced Pigment Recovery" Journal of Fungi 3, no. 3: 33. https://doi.org/10.3390/jof3030033