Abstract
It is generally accepted that Monascus pigments are predominantly cell-bound, including both intracellular and surface-bound pigments. This long-term misconception was corrected in the present work. Production of extracellular crystal pigments by submerged culture of Monascus sp. was confirmed by microscopic observation and collection of Monascus pigments from extracellular broth by direct membrane filtration. Following up the new fact, the bioactivity of mycelia as whole-cell biocatalyst for biosynthesis and biodegradation of Monascus pigments had been detailedly examined in both an aqueous solution and a nonionic surfactant micelle aqueous solution. Based on those experimental results, cell suspension culture in an aqueous medium was developed as a novel strategy for accumulation of high concentration of Monascus pigments. Thus, glucose feeding during submerged culture in the aqueous medium was carried out successfully and high orange Monascus pigments concentration of near 4 g/L was achieved.
Similar content being viewed by others
References
Abbasnezhad H, Gray M, Foght JM (2011) Influence of adhesion on aerobic biodegradation and bioremediation of liquid hydrocarbons. Appl Microbiol Biotechnol 92:653–675
Achard M, Beeler AB, Jr Porco JA (2012) Synthesis of azaphilone-based chemical libraries. ACS Comb Sci 14:236–244
Andryushina VA, Rodina NV, Stytsenko TS, Huy LD, Druzhinina AV, Yaderetz VV, Voishvillo NE (2011) Conversion of soybean sterols into 3, 17-diketosteroids using Actinobacteria Mycobacterium neoaurum, Pimelobacter simplex, and Rhodococcus erythropolis. Appl Biochem Microbiol 47(3):270–273
Balakrishnan B, Karki S-H, Chiu S-H, Kim H-J, Suh J-W, Nam B, Yoon Y-M, Chen C-C, Kwon H-J (2013) Genetic localization and in vivo characterization of a Monascus azaphilone pigment biosynthetic gene cluster. Appl Microbiol Biotechnol 97:6337–6345
Balakrishnan B, Park S-H, Kwon H-J (2017a) A reductase gene mppE controls yellow component production in azaphilone polyketide pathway of Monascus. Biotechnol Lett 39(1):163–169
Balakrishnan B, Park S-H, Kwon H-J (2017b) Inactivation of the oxidase gene mppG results in the selective loss of orange azaphilone pigments in Monascus purpureus. Appl Biol Chem 60(4):437–446
Chen G, Shi K, Song D, Quan L, Wu Z (2015) The pigment characteristics and productivity shifting in high cell density culture of Monascus anka mycelia. BMC Biotechnol 15:72. https://doi.org/10.1186/s12896-015-0183-3
Chen W, Chen R, Liu Q, He Y, He K, Ding X, Kang L, Guo X, Xie N, Zhou Y, Lu Y, Cox RJ, Molnar I, Li M, Shao Y, Chen F (2017a) Orange, red, yellow: biosynthesis of azaphilone pigments in Monascus fungi. Chem Sci 8:4917–4925
Chen G, Huang T, Bei Q, Tian X, Wu Z (2017b) Correlation of pigment production with mycelium morphology in extractive fermentation of Monascus anka GIM 3.592. Process Biochem 58:42–50
Chiu S-W, Poon Y-K (1993) Submerged production of Monascus pigments. Mycologia 85(2):214–218
Choe D, Lee J, Woo S, Shin CS (2012) Evaluation of the amine derivatives of Monascus pigment with anti-obesity activities. Food Chem 134:315–323
Evans PJ, Wang HY (1984) Pigment production from immobilized Monascus sp. utilizing polymeric resin adsorption. Appl Environ Microbiol 47(6):1323–1326
Feng Y, Shao Y, Chen F (2012) Monascus pigments. Appl Microbiol Biotechnol 96:1421–1440
Gao J-M, Yang S-X, Qin J-C (2013) Azaphilones: chemistry and biology. Chem Rev 113:4755–4811
Gomes DC, Takahashi JA (2016) Sequential fungal fermentation-biotransformation process to produce a red pigment from sclerotiorin. Food Chem 210:355–361
Hajjaj H, Klaebe A, Loret MO, Tzedakis T, Goma G, Blanc PJ (1997) Production and identification of N-glucosylrubropunctamine and N-glucosylmonascorbramine from Monascus ruber and occurrence of electron donor-acceptor complex in these red pigments. Appl Environ Microbiol 63:2671–2678
Hinze WL, Pramauro E (1993) A critical review of surfactant-mediated phase separations (cloud-point extraction): theory and applications. Criti Rev Anal Chem 24:133–177
Hu Z, Zhang X, Wu Z, Qi H, Wang Z (2012) Perstraction of intracellular pigments by submerged cultivation of Monascus in nonionic surfactant micelle aqueous solution. Appl Microbiol Biotechnol 94:81–89
Jung H, Kim C, Kim K, Shin CS (2003) Color characteristics of Monascus pigments derived by fermentation with various amino acids. J Agric Food Chem 51:1302–1306
Kang B, Zhang X, Wu Z, Qi H, Wang Z (2013) Effect of pH and nonionic surfactant on profile of intracellular and extracellular Monascus pigments. Process Biochem 48:759–767
Kolia SH, Suryawanshia RK, Patilac CD, Patil SV (2017) Fluconazole treatment enhances extracellular release of red pigments in the fungus Monascus purpureus FEMS Microbiol Lett 364 https://doi.org/10.1093/femsle/fnx058
Lin C-F, Lizuka H (1982) Production of extracellular pigment by a mutant of Monascus kaoliang sp. nov. Appl Environ Microbiol 43(3):671–676
Lin TF, Demain AL (1991) Effect of nutrition of Monascus sp. on formation of red pigments. Appl Microbiol Biotechnol 36:70–75
Lu F, Huang Y, Zhang X, Wang Z (2017) Biocatalytic activity of Monascus mycelia depending on physiology and high sensitivity to product concentration. AMB Expr 7:88. https://doi.org/10.1186/s13568-017-0391-4
Ma J, Li Y, Ye Q, Li J, Hua Y, Ju D, Zhang D, Cooper R, Chang M (2000) Constituents of red yeast rice, a traditional Chinese food and medicine. J Agric Food Chem 48:5220–5225
Mapari SAS, Thrane U, Meyer AS (2010) Fungal polyketide azaphilone pigments as future natural food colorants? Trends Biotechnol 28:300–307
Vendruscolo F, Tosin I, Giachini AJ, Schmidell W, Ninow JL (2014) Antimicrobial activity of Monascus pigments produced in submerged culture. J Food Process Pres 38:1860–1865
Vendruscolo F, Schmidell W, Moritz DE, Bühler RMM, Oliveira D, Ninow JL (2016) Isoelectric point of amino acid: Importance for Monascus pigment production. Biocatal Agri Biotechnol 5:179–185
Wang B, Zhang X, Wu Z, Wang Z (2016) Biosynthesis of Monascus pigments by resting cell submerged culture in nonionic surfactant micelle aqueous solution. Appl Microb Biotechnol 100(16):7083–7089
Wang Y, Zhang B, Lu L, Huang Y, Xu G (2013) Enhanced production of pigments by addition of surfactants in submerged fermentation of Monascus purpureus H1102. J Sci Food Agric 93:3339–3344
Wang Z (2007) The potential of cloud point system as a novel two-phase partitioning system for biotransformation. Appl Microbiol Biotechnol 75:1–10
Wang Z (2011) Bioavailability of organic compound solubilized in nonionic surfactant micelles. Appl Microbiol Biotechnol 89:523–534
Wang Z, Dai Z (2010) Extractive microbial fermentation in cloud point system. Enzym Microb Technol 46:407–418
Wong H, Koehler PE (1983) Production of red water-soluble Monascus pigments. J Food Sci 48:1200–1203
Xiong X, Zhang X, Wu Z, Wang Z (2015a) Coupled aminophilic reaction and directed metabolic channeling to red Monascus pigments by extractive fermentation in nonionic surfactant micelle aqueous solution. Process Biochem 50(2):180–187
Xiong X, Zhang X, Wu Z, Wang Z (2015b) Accumulation of yellow Monascus pigments by extractive fermentation in nonionic surfactant micelle aqueous solution. Appl Microbiol Biotechnol 99(3):1173–1180
Xue Y, Qian C, Wang Z, Xu J-H, Yang Y, Qi H (2010) Investigation of extractive microbial transformation in direct nonionic surfactant micelle aqueous solution by response surface methodology. Appl Microbiol Biotechnol 85(1):517–524
Zheng Y, Xin Y, Guo Y (2009) Study on the fingerprint profile of Monascus products with HPLC-FD, FAD and MS. Food Chem 113:705–711
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict interests.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Electronic supplementary material
ESM 1
(PDF 701 kb)
Rights and permissions
About this article
Cite this article
Lu, F., Liu, L., Huang, Y. et al. Production of Monascus pigments as extracellular crystals by cell suspension culture. Appl Microbiol Biotechnol 102, 677–687 (2018). https://doi.org/10.1007/s00253-017-8646-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-017-8646-1