Research and Innovation in Food Science and Technology

Effect of Saccharomyces cerevisiae Live Cell and Treated with Heat and Acid on Citrinin and Pigments of Monascus purpureus

Document Type : Original Paper

Authors

1 PhD. Student, Department of Food Science and Technology, Ferdowsi University of Mashhad, Mashhad, Iran

2 Professor, Department of Food Science and Technology, Ferdowsi University of Mashhad, Mashhad, Iran

3 Associated Professor, Department of Biotechnology, Research Institute of Food Science and Technology, Mashhad, Iran

4 Professor, Department of Chemistry, Payame Noor University, Mashhad, Iran

Abstract

Monascus purpureus can produce a wide range of natural pigments so attract the attention of food producers as substitute of synthetic colors. Monascus pigments usually accompanied with citrinin contamination which limits their wide application in foods. The usage of Saccharomyces cerevisiae is known as a useful biological way for citrinin elimination. In this study, the effect of  Saccharomyces cerevisiae cells in twomodes of treatment (heat treatment at 121  °C and acid treatment in 2M HCL) and live at three different concentrations (103, 104, 105 CFU/mL) were investigated on the amount of citrinin and yellow, orange and red pigments produced by Monascus purpureus. The results showed that live yeast cell and yeast cells treated by heat and acid significantly decreased the citrinin in culture, so that citrinin content decreased from 4.43 mg/L in control sample to 0.9, 0.10 and 0.07 mg/L (at 105 CFU/mL yeast suspension) respectively. The maximum amount of yellow, orange and red extracellular and intracellular measured pigments belong to the samples with live yeast, while the amount of this pigments in the samples containing yeast treated with heat and acid reduced respectively. Among the treatments, the use of live yeast at concentration of 104 CFU/mL per milliliter provided the best conditions to achieve the desired goal.

Keywords

Al-Sarrani, A. Q. M., & El-Naggar, M. Y. M. (2006). Application of Plackett-Burman factorial design to improve citrinin production in Monascus rubber batch cultures. Botanical Studies, 47, 167-174.
Armando, M., Pizzolitto, R., Dogi, C., Cristofolini, A., Merkis, C., Poloni, V., . . . Cavaglieri, L. (2012). Adsorption of ochratoxin A and zearalenone by potential probiotic Saccharomyces cerevisiae strains and its relation with cell wall thickness. Journal of applied microbiology, 113(2), 256-264. doi:https://doi.org/10.1111/j.1365-2672.2012.05331.x
Avazpour, M., Seifipour, F., Abdi, J., Nabavi, T., & Zamanian-Azodi, M. (2013). Detection of dyes in confectionery products using thin-layer chromatography. Iranian Journal of Nutrition Sciences & Food Technology, 8(3), 73-78.  (in Persian)
Bejaoui, H., Mathieu, F., Taillandier, P., & Lebrihi, A. (2004). Ochratoxin A removal in synthetic and natural grape juices by selected oenological Saccharomyces strains. Journal of applied microbiology, 97(5), 1038-1044.
Blanc, P., Loret, M., & Goma, G. (1995). Production of citrinin by various species ofMonascus. Biotechnology Letters, 17(3), 291-294. doi:https://doi.org/10.1007/BF01190639
Bueno, D. J., Casale, C. H., Pizzolitto, R. P., Salvano, M. A., & Oliver, G. (2007). Physical adsorption of aflatoxin B1 by lactic acid bacteria and Saccharomyces cerevisiae: a theoretical model. Journal of food protection, 70(9), 2148-2154. doi:https://doi.org/10.4315/0362-028X-70.9.2148
Chen, D., Xue, Y., Chen, M., Li, Z., & Wang, C. (2016). Optimization of submerged fermentation medium for citrinin-free monascin production by Monascus. Preparative Biochemistry and Biotechnology, 46(8), 772-779. doi:https://doi.org/10.1080/10826068.2015.1135461
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 biotechnology, 15(1), 1-9. doi:https://doi.org/10.1186/s12896-015-0183-3
Dikshit, R., & Tallapragada, P. (2011). Monascus purpureus: A potential source for natural pigment production. Journal of Microbiology and Biotechnology Research, 1(4), 164-174.
Duraklı-Velioğlu, S., Boyacı, İ. H., Şimşek, O., & Gümüş, T. (2013). Optimizing a submerged Monascus cultivation for production of red pigment with bug damaged wheat using artificial neural networks. Food Science and Biotechnology, 22(6), 1639-1648. doi:https://doi.org/10.1007/s10068-013-0261-z
Hamdi, M., Blanc, P., Loret, M., & Goma, G. (1997). A new process for red pigment production by submerged culture of Monascus purpureus. Bioprocess Engineering, 17(2), 75-79. doi:https://doi.org/10.1007/PL00008958
Jia, X. Q., Xu, Z. N., Zhou, L. P., & Sung, C. K. (2010). Elimination of the mycotoxin citrinin production in the industrial important strain Monascus purpureus SM001. Metabolic engineering, 12(1), 1-7. doi:https://doi.org/10.1016/j.ymben.2009.08.003
Karazhiyan, H., Mehraban Sangatash, M., Karazhyan, R., Mehrzad, A., & Haghighi, E. (2016). Ability of different treatments of Saccharomyces cerevisiae to surface bind aflatoxin M1 in yoghurt. Journal of Agricultural Science and Technology, 18(6), 1489-1498.
Kobylewski, S., & Jacobson, M. F. (2012). Toxicology of food dyes. International journal of occupational and environmental health, 18(3), 220-246. doi:https://doi.org/10.1179/1077352512Z.00000000034
Kongruang, S. (2011). Growth kinetics of biopigment production by Thai isolated Monascus purpureus in a stirred tank bioreactor. Journal of industrial microbiology & biotechnology, 38(1), 93-99. doi:https://doi.org/10.1007/s10295-010-0834-2
Kurniawati, S., & Zubaidah, E. (2014). Enhanced Production of Red Pigment and Lovastatin by Co-Culture with Saccharomyces cereviciae in Angkak Rice-Mung Bean. International Journal of Technical Research and Application, 2(5), 64-67.
Li, J.-J., Shang, X.-Y., Li, L.-L., Liu, M.-T., Zheng, J.-Q., & Jin, Z.-L. (2010). New cytotoxic azaphilones from Monascus purpureus-fermented rice (red yeast rice). Molecules, 15(3), 1958-1966. doi:https://doi.org/10.3390/molecules15031958
Lin, T., Yakushijin, K., Büchi, G., & Demain, A. (1992). Formation of water-solubleMonascus red pigments by biological and semi-synthetic processes. Journal of Industrial Microbiology, 9(3-4), 173-179. doi:https://doi.org/10.1007/BF01569621
Malik, K., Tokkas, J., & Goyal, S. (2012). Microbial pigments: a review. International Journal of Microbial Resource Technology, 1(4), 361-365.
Manan, M., Mohamad, R., & Ariff, A. (2017). Monascus spp.: A source of Natural Microbial Color through Fungal Biofermentation. Journal of Microbiology & Experimentation, 5(3), 00148. doi:https://doi.org/10.15406/jmen.2017.05.00148
Morata, A., Loira, I., & Suárez Lepe, J. (2016). Influence of yeasts in wine colour. Grape and Wine Biotechnology; Morata, A., Loira, I., Eds. 285-305
Mu, H., Huang, L., Ding, X., & Zhao, S. (2015). Influence of different substrates on the production of pigments and citrinin by Monascus FJ46. In Advances in Applied Biotechnology (pp. 257-264): Springer, Berlin, Heidelberg.
Nadzri, N. S. (2012). The optimization of red pigment by Monascus purpureus FTC 5356 in solid state fermentation. (Doctoral dissertation), Universiti Malaysia Pahang, Retrieved from https://www.semanticscholar.org/paper/The-optimization-of-red-pigment-by-monascus-FTC-in-Shazwani/8cd6570e4f56849847ae042ba09693b3c4eaf0f1?p2df
NCCLS, N. (2002). Reference method for broth dilution antifungal susceptibility testing of yeasts; Approved standard. In (Second ed.): NCCLS, 940 West Valley Road, Suite 1400, NCCLS Wayne, PA, USA.
Orozco, S. F. B., & Kilikian, B. V. (2008). Effect of pH on citrinin and red pigments production by Monascus purpureus CCT3802. World Journal of Microbiology and Biotechnology, 24(2), 263-268. doi:https://doi.org/10.1007/s11274-007-9465-9
Patakova, P. (2013). Monascus secondary metabolites: production and biological activity. Journal of industrial microbiology & biotechnology, 40(2), 169-181. doi:https://doi.org/10.1007/s10295-012-1216-8
Piotrowska, M. (2011). Adsorption of ochratoxin A by Saccharomyces cerevisiae living and non-living cells. Acta alimentaria, 41(1), 1-7. doi:https://doi.org/10.1556/aalim.2011.0006
Rahaie, S., Emam-Djomeh, Z., Razavi, S., & Mazaheri, M. (2010). Immobilized Saccharomyces cerevisiae as a potential aflatoxin decontaminating agent in pistachio nuts. Brazilian Journal of Microbiology, 41(1), 82-90.
Said, F. (2010). Monascus ruber ICMP 15220 Fermentation for the Production of Pigment. (Doctoral dissertation), Massey University, New Zealand, Retrieved from https://mro.massey.ac.nz/bitstream/handle/10179/2654/02_whole.pdf
Satapa, N. A. A. (2013). Optimization of Yellow Pigment Production by Monascus Purpureus from Banana Peel. (Doctoral dissertation), Universiti Malaysia Pahang, Retrieved from http://umpir.ump.edu.my/id/eprint/7220/1/Optimization_of_yellow_pigment_production.pdf
Seyedin, A., Hatamian-Zarmi, A., Rasekh, B., & Mirderikvand, M. (2015). Natural Pigment Production by Monascus purpureus: Bioreactor Yield Improvement through Statistical Analysis. Applied Food Biotechnology, 2(2), 23-30. doi:https://doi.org/10.22037/afb.v2i2.7457
Shetty, P. H., Hald, B., & Jespersen, L. (2007). Surface binding of aflatoxin B 1 by Saccharomyces cerevisiae strains with potential decontaminating abilities in indigenous fermented foods. International journal of food microbiology, 113(1), 41-46. doi:https://doi.org/10.1016/j.ijfoodmicro.2006.07.013
Shetty, P. H., & Jespersen, L. (2006). Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trends in Food Science & Technology, 17(2), 48-55. doi:https://doi.org/10.1016/j.tifs.2005.10.004
Shin, C. S., Kim, H. J., Kim, M. J., & Ju, J. Y. (1998). Morphological change and enhanced pigment production of Monascus when cocultured with Saccharomyces cerevisiae or Aspergillus oryzae. Biotechnology and bioengineering, 59(5), 576-581. doi:https://doi.org/10.1002/(SICI)1097-0290(19980905)59:53.0.CO;2-7
Suh, J.-H., & Shin, C. S. (2000a). Analysis of the morphologic changes of Monascus sp. J101 cells cocultured with Saccharomyces cerevisiae. FEMS Microbiology Letters, 193(1), 143-147. doi:https://doi.org/10.1111/j.1574-6968.2000.tb09416.x
Suh, J.-H., & Shin, C. S. (2000b). Physiological analysis on novel coculture of Monascus sp. J101 with Saccharomyces cerevisiae. FEMS Microbiology Letters, 190(2), 241-245. doi:https://doi.org/10.1111/j.1574-6968.2000.tb09293.x
Suharna, N. (2015). Production of Non Citrinin Chinese Red Yeast Rice by Using Monascus purpureus Skw2 Co-cultured with Bacillus megaterium. International Journal of Advanced Research in Biological Sciences, 2(2), 72-78. doi:https://doi.org/10.5072/RIN/SDWT8R
Wang, H., Zhang, S., Lin, T., & Zheng, D. (2017). Introduction and safety evaluation of citrinin in foods. Journal of Food and Nutrition Sciences, 5(5), 179-183. doi:https://doi.org/10.11648/j.jfns.20170505.13
Wang, S., Zhao, S., Mu, H., Sun, F., & Chen, P. (2014). Effect of Lactococcus lactis subsp. on Production of Pigment and Citrinin by Monascus. Paper presented at the Proceedings of the 2012 International Conference on Applied Biotechnology (ICAB 2012).
Wang, Y.-Z., Ju, X.-L., & Zhou, Y.-G. (2005). The variability of citrinin production in Monascus type cultures. Food Microbiology, 22(1), 145-148. doi:https://doi.org/10.1016/j.fm.2004.01.006
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. Journal of the Science of Food and Agriculture, 93(13), 3339-3344. doi:https://doi.org/10.1002/jsfa.6182
Xiong, X., Zhang, X., Wu, Z., & Wang, Z. (2014). Optimal selection of agricultural products to inhibit citrinin production during submerged culture of Monascus anka. Biotechnology and bioprocess engineering, 19(6), 1005-1013. doi:https://doi.org/10.1007/s12257-014-0419-4
Zhang, L., Li, Z., Dai, B., Zhang, W., & Yuan, Y. (2013). Effect of submerged and solid-state fermentation on pigment and citrinin production by Monascus purpureus. Acta Biologica Hungarica, 64(3), 385-394. doi:https://doi.org/10.1556/abiol.64.2013.3.11
Zhou, B., Zhu, M.-J., Wang, J.-F., Wu, Z.-Q., & Liang, S.-Z. (2009). Effect of Ammonium Salts on Monascus Yellow and Red Pigments and Citrinin Production. Journal of Chongqing Institute of Technology (Natural Science), 1, 010.
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Research and Innovation in Food Science and Technology
Volume 9, Issue 3
October 2020
Pages 255-268
  • Receive Date: 15 July 2019
  • Revise Date: 20 April 2020
  • Accept Date: 20 June 2020