Optimizing Medium Compositions and Bioreactor Conditions to Improve and Cost-effectively Produce Monascus purpureus Pigments

Document Type : Research Paper

Authors

Department of Horticultural Science and Landscape, Faculty of Agriculture, Ferdowsi University of Mashhad (FUM), Mashhad, Iran

Abstract

Bio pigments produced by Monascus spp. have potential applications mainly in the food and medical industries. In the present study, a two-step statistical method was used to optimize the production of yellow, orange, and red pigments from Monascus purpureus. Eleven independent variables, including four carbon sources (wheat, barley, rice, and potato extracts), two nitrogen sources (ammonium nitrate and urea), nutrient elements (P, K, and microelements), and four bioreactor conditions (temperature, aeration, stirring, and pH) were optimized through Plackett-Burman design (PBD) and response surface method (RSM) methods. The model for each pigment was constructed and validated. With regard to carbon sources, the highest level of pigments was achieved at 2 g/l of rice and 9 g/l barley for yellow pigment, 2 g/l of rice and 18 g/l of barley for orange pigment, and 18 g/l of rice and 18 g/l wheat for red pigments. Temperature and barley extracts triggered the production of yellow pigments. The orange pigment was increased by pH and barley. Rice and wheat have a positive significant influence on red pigments. Aeration, pH, and stirring increased the production of the pigment. Citrinin is a biotoxin produced by Monascus during the fermentation process. The concentration of citrinin varied from 0.054 to 0.135 (μg/mL). The lowest amount of citrinin was achieved at 2 L/Min aeration or 6 L/Min stirring. This system is critical for the bioprocess, as it inhibits the citrinin product, and it could be a promising step in increasing pigment yield.

Keywords


  1. Agboyibor C., Kong W.B., Chen D., Zhang A.M., Niu S.Q. Monascus pigments production, composition, bioactivity and its application: A review. Biocatalysis and agricultural biotechnology. 2018;16:433-47.
  2. Tarakemeh A., Azizi M., Rowshan V., Salehi H., Spina R., Dupire F., et al. Screening of Amaryllidaceae alkaloids in bulbs and tissue cultures of Narcissus papyraceus and four varieties of N. tazetta. Journal of Pharmaceutical and Biomedical Analysis. 2019;172:230-7.
  3. Lin Y.L., Wang T.H., Lee M.H., Su N.W. Biologically active components and nutraceuticals in the Monascus-fermented rice: a review. Applied microbiology and biotechnology. 2008;77(5):965-73.
  4. Xiong X., Zhang X., Wu Z., Wang Z. Coupled aminophilic reaction and directed metabolic channeling to red Monascus pigments by extractive fermentation in nonionic surfactant micelle aqueous solution. Process Biochemistry. 2015;50(2):180-7.
  5. Lv J, Zhang B.B., Liu X.D., Zhang C., Chen L., Xu G.R., et al. Enhanced production of natural yellow pigments from Monascus purpureus by liquid culture: The relationship between fermentation conditions and mycelial morphology. Journal of bioscience and bioengineering. 2017;124(4):452-8.
  6. Stoev S.D. Foodborne mycotoxicoses, risk assessment and underestimated hazard of masked mycotoxins and joint mycotoxin effects or interaction. Environmental toxicology and pharmacology. 2015;39(2):794-809.
  7. Embaby A.M., Hussein M.N., Hussein A. Monascus orange and red pigments production by Monascus purpureus ATCC16436 through co-solid state fermentation of corn cob and glycerol: An eco-friendly environmental low cost approach. PLoS One. 2018;13(12): e0207755.
  8. Srianta I., Zubaidah E., Estiasih T., Yamada M. Comparison of Monascus purpureus growth, pigment production and composition on different cereal substrates with solid state fermentation. Biocatalysis and Agricultural Biotechnology. 2016;7:181-6.
  9. Da Costa J.P.V., Vendruscolo F. Production of red pigments by Monascus ruber CCT 3802 using lactose as a substrate. Biocatalysis and agricultural biotechnology. 2017;11:50-5.
  10. Srivastav P., Yadav V.K., Govindasamy S., Chandrasekaran M. Red pigment production by Monascus purpureus using sweet potato-based medium in submerged fermentation. Nutrafoods. 2015;14(3):159-67.
  11. Subhasree R., Babu P.D., Vidyalakshmi R., Mohan V.C. Effect of carbon and nitrogen sources on stimulation of pigment production by Monascus purpureus on jackfruit seeds. International J Microbiological Research (IJMR). 2011;2(2):184-7.
  12. Patrovsky M, Sinovska K., Branska B., Patakova P. Effect of initial pH, different nitrogen sources, and cultivation time on the production of yellow or orange Monascus purpureus pigments and the mycotoxin citrinin. Food science & nutrition. 2019;7(11):3494-500.
  13. Asadian A.H., Azizi M., Arouiee H. Semi-industrial Production of Lovastatin with a Standard Amount of Mycotoxin Citrinin from Monascus purpureus. J Medicinal plants and By-product. 2022.
  14. Wang Y-Z, Ju X-L, Zhou Y-G. The variability of citrinin production in Monascus type cultures. Food Microbiology. 2005;22(1):145-8.
  15. Domínguez-Espinosa R.M., Webb C. Submerged fermentation in wheat substrates for production of Monascus pigments. World J microbiology and biotechnology. 2003;19(3):329-36.
  16. Azizi M., Tavana M., Farsi M., Oroojalian F. Yield performance of Lingzhi or Reishi medicinal mushroom, Ganoderma lucidum (W. Curt.: Fr.) P. Karst. (higher Basidiomycetes), using different waste materials as substrates. International J Medicinal Mushrooms. 2012;14(5).
  17. Liu J., Luo Y., Guo T, Tang C., Chai X., Zhao W., et al. Cost-effective pigment production by Monascus purpureus using rice straw hydrolysate as substrate in submerged fermentation. 2020;129(2):229-36.
  18. Velmurugan P., Hur H., Balachandar V., Kamala-Kannan S., Lee K.J., Lee S.M., et al. Monascus pigment production by solid-state fermentation with corn cob substrate. J bioscience and bioengineering. 2011;112(6):590-4.
  19. Liu J., Luo Y., Guo T., Tang C., Chai X., Zhao W., et al. Cost-effective pigment production by Monascus purpureus using rice straw hydrolysate as substrate in submerged fermentation. J bioscience and bioengineering. 2020;129(2):229-36.
  20. Silbir S., Goksungur Y. Natural red pigment production by Monascus purpureus in submerged fermentation systems using a food industry waste: Brewer’s spent grain. Foods. 2019;8(5):161.
  21. Hilares R.T., de Souza R.A., Marcelino P.F., da Silva S.S., Dragone G., Mussatto S.I., et al. Sugarcane bagasse hydrolysate as a potential feedstock for red pigment production by Monascus ruber. Food chemistry. 2018;245:786-91.
  22. Jirasatid S., Nopharatana M., Kitsubun P., Vichitsoonthonkul T., Tongta A. Statistical optimization for monacolin K and yellow pigment production and citrinin reduction by Monascus purpureus in solid-state fermentation. J microbiology and biotechnology. 2013;23(3):364-74.
  23. Fincher G. Morphology and chemical composition of barley endosperm cell walls. J the Institute of Brewing. 1975;81(2):116-22.
  24. Sharmila G., Nidhi B., Muthukumaran C. Sequential statistical optimization of red pigment production by Monascus purpureus (MTCC 369) using potato powder. Industrial Crops and Products. 2013;44:158-64.
  25. Sepelev I., Galoburda R. Industrial potato peel waste application in food production: a review. Research for Rural Development. 2015;1:130-6.
  26. Lin T., Demain A. Negative effect of ammonium nitrate as nitrogen source on the production of water-soluble red pigments by Monascus sp. Applied microbiology and biotechnology. 1995;43(4):701-5.
  27. Zhou B., Wang Y., Lu H., Zhou Y. Effect of ammonium salts on pigments production by Monascus anka mutant in 5L bioreactor. Chiang Mai J Sci. 2014;41:1032-43.
  28. Shahhoseini R., Azizi M., Asili J., Moshtaghi N., Samiei L. Effects of zinc oxide nanoelicitors on yield, secondary metabolites, zinc and iron absorption of Feverfew (Tanacetum parthenium (L.) Schultz Bip.). Acta physiologiae plantarum. 2020;42:1-18.
  29. Heidari S., Azizi M., Soltani F., Hadian J. Foliar application of Ca (NO3) 2 and KNO3 affects growth, essential oil content, and oil composition of French tarragon. Industrial Crops and Products. 2014;62:526-32.
  30. Orozco S.F.B., Kilikian B.V. Effect of pH on citrinin and red pigments production by Monascus purpureus CCT3802. World J Microbiology and Biotechnology. 2008;24(2):263-8.
  31. Carvalho J.C.d., Oishi B.O., Pandey A., Soccol C.R. Biopigments from Monascus: strains selection, citrinin production and color stability. Brazilian Archives of Biology and Technology. 2005;48:885-94.
  32. Roussos S., Lonsane B., Raimbault M., Viniegra-Gonzalez G. Advances in solid state fermentation: Springer Science & Business Media; 2013.
  33. Kang B., Zhang X., Wu Z., Wang Z., Park S. Production of citrinin-free Monascus pigments by submerged culture at low pH. Enzyme and microbial technology. 2014;55:50-7.