Antioxidant properties and production of monacolin k, citrinin, and red pigments during solid state fermentation of purple rice (Oryzae sativa) varieties by Monascus purpureus

https://doi.org/10.17221/154/2016-CJFSCitation:Pengnoi P., Mahawan R., Khanongnuch C., Lumyong S. (2017): Antioxidant properties and production of monacolin k, citrinin, and red pigments during solid state fermentation of purple rice (Oryzae sativa) varieties by Monascus purpureus. Czech J. Food Sci., 35: 32-39.
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This study aims to evaluate the effects of various purple rice varieties on the production of monacolin K, citrinin, and red pigments by Monascus purpureus CMU002U (UV-mutant strain) and their antioxidant properties. The lowest value of citrinin concentration (132 ppb) was found in the SSF of the Na variety, which passed the standards of Japan, Taiwan, and European Union. The high monacolin K (13 482 ppm) and red pigment (388.25 units/g) levels were obtained from the fermented Doi Muser variety. The lowest IC50 value of the DPPH assay was found in the extract of fermented Doi Saked variety. An investigation of temperature shifting of the SSF for the Doi Muser variety indicated that the incubation at 30°C for 5 days, followed by 25°C until 30 days, yielded the highest value of monacolin K (35 292 ppm) production. These results demonstrated that fermented purple rice has a high potential to be developed as a new food supplement.
References:
Al-Shahrani Mesfer Mohammed (2013): Measurement of Antioxidant Activity in Selected Food Products and Nutraceuticals. Journal of Nutrition & Food Sciences, 03, - https://doi.org/10.4172/2155-9600.1000205
 
Ansorge M. B., Kula M. R. (2000): Investigating expression systems for the stable large-scale production of recombinant L -leucine-dehydrogenase from Bacillus cereus in Escherichia coli. Applied Microbiology and Biotechnology, 53, 668-673 https://doi.org/10.1007/s002539900290
 
Babu P.D., Subhasree R.S., Bhakyaraj R., Vidhyalakshmi R. (2009): Brown rice-beyond the color reviving a lost health food – a review. American-Eurasian Journal of Agronomy, 2: 67–72.
 
Betina V. (1989): Mycotoxin. Chemical, Biological and Environmental Aspects. Amsterdam, Elsevier.
 
Blanc P.J., Hajjai H., Loret M.O., Gomas G. (1998): Control of the production of citrinin by Monascus. In: Proceedings of the Symposium on Monascus Culture and Applications, July 8–10, 1998, Toulouse, France.
 
Brand-Williams W., Cuvelier M.E., Berset C. (1995): Use of a free radical method to evaluate antioxidant activity. LWT - Food Science and Technology, 28, 25-30 https://doi.org/10.1016/S0023-6438(95)80008-5
 
Campoy Sonia, Rumbero Angel, Martín Juan F., Liras Paloma (2006): Characterization of an hyperpigmenting mutant of Monascus purpureus IB1: identification of two novel pigment chemical structures. Applied Microbiology and Biotechnology, 70, 488-496 https://doi.org/10.1007/s00253-005-0090-y
 
Carvalho J.C., Oishi B.O., Woiciechowski A.L., Pandey A., Babitha S., Soccol C.R. (2007): Effect of substrates on the production of Monascus biopigments by solid-state fermentation and pigment extraction using different solvents. Indian Journal of Biotechnology, 6: 194–199.
 
Chairote E., Chairote G., Wongpornchai S., Lumyong S. (2007): Preparation of red yeast rice using various Thai glutinous rice and Monascus purpureus CMU001 isolated from commercial Chinese red yeast rice sample. KMITL Science Journal, 7: 28–37.
 
Chairote E.O., Chairote G., Lumyong S. (2009): Red yeast rice prepared from Thai glutinous rice, the antioxidant activities. Chiang Mai Journal of Science, 36: 42–49.
 
Childress Lindsey, Gay Andrea, Zargar Atanaz, Ito Matthew K. (2013): Review of red yeast rice content and current Food and Drug Administration oversight. Journal of Clinical Lipidology, 7, 117-122 https://doi.org/10.1016/j.jacl.2012.09.003
 
Chen Pei-Ni, Chu Shu-Chen, Chiou Hui-Ling, Chiang Chui-Liang, Yang Shun-Fa, Hsieh Yih-Shou (2005): Cyanidin 3-Glucoside and Peonidin 3-Glucoside Inhibit Tumor Cell Growth and Induce Apoptosis In Vitro and Suppress Tumor Growth In Vivo. Nutrition and Cancer, 53, 232-243 https://doi.org/10.1207/s15327914nc5302_12
 
Chiu Chiu-Hsia, Ni Kuang-Huei, Guu Yuan-Kuang, Pan Tzu-Ming (2006): Production of red mold rice using a modified Nagata type koji maker. Applied Microbiology and Biotechnology, 73, 297-304 https://doi.org/10.1007/s00253-006-0457-8
 
Chung C.C., Huang T.C., Chen H.H. (2009): The optimization of Monascus fermentation process for pigments increment and citrinin reduction. In: Bioinformatics and Bioengineering, 2009 IEEE International Conference, June 22–24, 2009, Taichung, Taiwan: 77–83.
 
European Commission (2014): Commission Regulation (EU) No 212/2014 of 6 March 2014 amending Regulation (EC) No 1881/2006 as regards maximum levels of the contaminant citrinin in food supplements based on rice fermented with red yeast Monascus purpureus. Available at http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=OJ:L:2014:067:TOC (accessed Oct 3, 2016).
 
FABRE C. E., SANTERRE A. L., LORET M. O., BABERIAN R., PAREILLEUX A., GOMA G., BLANC P.J. (1993): Production and Food Applications of the Red Pigments of Monascus ruber. Journal of Food Science, 58, 1099-1102 https://doi.org/10.1111/j.1365-2621.1993.tb06123.x
 
Feng Yanli, Shao Yanchun, Zhou Youxiang, Chen Fusheng (2014): Monacolin K production by citrinin-free Monascus pilosus MS-1 and fermentation process monitoring. Engineering in Life Sciences, , n/a-n/a https://doi.org/10.1002/elsc.201300128
 
Fernando Binosha (2013): Rice as a Source of Fibre. Rice Research: Open Access, 1, - https://doi.org/10.4172/jrr.1000e101
 
Journoud Mélanie, Jones Peter J.H (2004): Red yeast rice: a new hypolipidemic drug. Life Sciences, 74, 2675-2683 https://doi.org/10.1016/j.lfs.2003.10.018
 
Kalaivani M., Rajasekaran A. (2014): Improvement of monacolin K/citrinin production ratio in Monascus purpureus using UV mutagenesis. Nutrafoods, 13, 79-84 https://doi.org/10.1007/s13749-014-0021-6
 
Le Bloc’h J., Pauquai T., Bourges C. (2015): Authorised EU health claim for red yeast rice. In: Sadler M. (ed.): Foods, Nutrients and Food Ingredients with Authorised EU Health Claims: Volume 2. Elsevier B.V.: 139–142.
 
Lin Yii-Lih, Wang Teng-Hsu, Lee Min-Hsiung, Su Nan-Wei (2008): Biologically active components and nutraceuticals in the Monascus-fermented rice: a review. Applied Microbiology and Biotechnology, 77, 965-973 https://doi.org/10.1007/s00253-007-1256-6
 
Mienda B.S., Idi A., Umar A. (2011): Microbiological features of solid state fermentation and its applications – an overview. Research in Biotechnology, 2: 21–26.
 
Nimnoi Pongrawee, Lumyong Saisamorn (2011): Improving Solid-State Fermentation of Monascus purpureus on Agricultural Products for Pigment Production. Food and Bioprocess Technology, 4, 1384-1390 https://doi.org/10.1007/s11947-009-0233-8
 
Oh Chan-Ho, Oh Suk-Heung (2004): Effects of Germinated Brown Rice Extracts with Enhanced Levels of GABA on Cancer Cell Proliferation and Apoptosis. Journal of Medicinal Food, 7, 19-23 https://doi.org/10.1089/109662004322984653
 
Panlasigui >Leonora N., Thompson Lilian U. (2006): Blood glucose lowering effects of brown rice in normal and diabetic subjects. International Journal of Food Sciences and Nutrition, 57, 151-158 https://doi.org/10.1080/09637480500410879
 
Park Ji-Young, Han Sang-Ik, Seo Woo Duck, Ra Ji-Eun, Sim Eun-Yeong, Nam Min-Hee (2014): Study on Monascus Strains and Characteristic for Manufacturing Red Yeast Rice with High Production of Monacolin K. Korean Journal of Crop Science, 59, 167-173 https://doi.org/10.7740/kjcs.2014.59.2.167
 
Patil Swati Bhauso, Khan Md. Khalid (2011): Germinated brown rice as a value added rice product: A review. Journal of Food Science and Technology, 48, 661-667 https://doi.org/10.1007/s13197-011-0232-4
 
Rajasekaran Aiyalu, Kalaivani Muthusamy (2012): Biofortification of Indian rice (IR-532-E-576) with monacolin K by RSM optimisation using Monascus purpureus MTCC 1090. Nutrafoods, 11, 49-54 https://doi.org/10.1007/s13749-012-0031-1
 
Shi Yeu-Ching, Pan Tzu-Ming (2011): Beneficial effects of Monascus purpureus NTU 568-fermented products: a review. Applied Microbiology and Biotechnology, 90, 1207-1217 https://doi.org/10.1007/s00253-011-3202-x
 
Songsermsakul P. (2015): Mycotoxins contamination of food in Thailand (2000–2010): Food safety concerns for the world food exporter. International Food Research Journal, 22: 426–434.
 
Su Yuan-Chi, Wang Jyh-Jye, Lin Tzu-Tsen, Pan Tzu-Ming (2003): Production of the secondary metabolites γ-aminobutyric acid and monacolin K by Monascus. Journal of Industrial Microbiology & Biotechnology, 30, 41-46 https://doi.org/10.1007/s10295-002-0001-5
 
Subsaendee T., Kitpreechavanich V., Yongsmith B. (2014): Growth, glucoamylase, pigments and monacolin K production on rice solid culture in flask and koji chamber using Monascus sp. KB9. Chiang Mai Journal of Science, 41: 1044–1057.
 
Tsukahara Masatoshi, Shinzato Naoya, Tamaki Yasutomo, Namihira Tomoyuki, Matsui Toru (2009): Red Yeast Rice Fermentation by Selected Monascus sp. with Deep-Red Color, Lovastatin Production but No Citrinin, and Effect of Temperature-Shift Cultivation on Lovastatin Production. Applied Biochemistry and Biotechnology, 158, 476-482 https://doi.org/10.1007/s12010-009-8553-8
 
Velmurugan Palanivel, Hur Hyun, Balachandar Vellingiri, Kamala-Kannan Seralathan, Lee Kui-Jae, Lee Sang-Myung, Chae Jong-Chan, Shea Patrick J., Oh Byung-Taek (2011): Monascus pigment production by solid-state fermentation with corn cob substrate. Journal of Bioscience and Bioengineering, 112, 590-594 https://doi.org/10.1016/j.jbiosc.2011.08.009
 
Vidyalakshmi R., Paranthaman R., Murugesh S., Singaravadivel K. (2009): Stimulation of Monascus pigments by intervention of different nitrogen sources. Journal of Biotechnology and Biochemistry, 4: 25–28.
 
Wang Jyh-Jye, Lee Chung-Lin, Pan Tzu-Ming (2004): Modified Mutation Method for Screening Low Citrinin-Producing Strains of Monascus purpureus on Rice Culture. Journal of Agricultural and Food Chemistry, 52, 6977-6982 https://doi.org/10.1021/jf049783o
 
Xu Bao-Jun, Wang Qi-Jun, Jia Xiao-Qin, Sung Chang-Keun (2005): Enhanced lovastatin production by solid state fermentation ofMonascus ruber. Biotechnology and Bioprocess Engineering, 10, 78-84 https://doi.org/10.1007/BF02931187
 
Al-Shahrani Mesfer Mohammed (2013): Measurement of Antioxidant Activity in Selected Food Products and Nutraceuticals. Journal of Nutrition & Food Sciences, 03, - https://doi.org/10.4172/2155-9600.1000205
 
Ansorge M. B., Kula M. R. (2000): Investigating expression systems for the stable large-scale production of recombinant L -leucine-dehydrogenase from Bacillus cereus in Escherichia coli. Applied Microbiology and Biotechnology, 53, 668-673 https://doi.org/10.1007/s002539900290
 
Babu P.D., Subhasree R.S., Bhakyaraj R., Vidhyalakshmi R. (2009): Brown rice-beyond the color reviving a lost health food – a review. American-Eurasian Journal of Agronomy, 2: 67–72.
 
Betina V. (1989): Mycotoxin. Chemical, Biological and Environmental Aspects. Amsterdam, Elsevier.
 
Blanc P.J., Hajjai H., Loret M.O., Gomas G. (1998): Control of the production of citrinin by Monascus. In: Proceedings of the Symposium on Monascus Culture and Applications, July 8–10, 1998, Toulouse, France.
 
Brand-Williams W., Cuvelier M.E., Berset C. (1995): Use of a free radical method to evaluate antioxidant activity. LWT - Food Science and Technology, 28, 25-30 https://doi.org/10.1016/S0023-6438(95)80008-5
 
Campoy Sonia, Rumbero Angel, Martín Juan F., Liras Paloma (2006): Characterization of an hyperpigmenting mutant of Monascus purpureus IB1: identification of two novel pigment chemical structures. Applied Microbiology and Biotechnology, 70, 488-496 https://doi.org/10.1007/s00253-005-0090-y
 
Carvalho J.C., Oishi B.O., Woiciechowski A.L., Pandey A., Babitha S., Soccol C.R. (2007): Effect of substrates on the production of Monascus biopigments by solid-state fermentation and pigment extraction using different solvents. Indian Journal of Biotechnology, 6: 194–199.
 
Chairote E., Chairote G., Wongpornchai S., Lumyong S. (2007): Preparation of red yeast rice using various Thai glutinous rice and Monascus purpureus CMU001 isolated from commercial Chinese red yeast rice sample. KMITL Science Journal, 7: 28–37.
 
Chairote E.O., Chairote G., Lumyong S. (2009): Red yeast rice prepared from Thai glutinous rice, the antioxidant activities. Chiang Mai Journal of Science, 36: 42–49.
 
Childress Lindsey, Gay Andrea, Zargar Atanaz, Ito Matthew K. (2013): Review of red yeast rice content and current Food and Drug Administration oversight. Journal of Clinical Lipidology, 7, 117-122 https://doi.org/10.1016/j.jacl.2012.09.003
 
Chen Pei-Ni, Chu Shu-Chen, Chiou Hui-Ling, Chiang Chui-Liang, Yang Shun-Fa, Hsieh Yih-Shou (2005): Cyanidin 3-Glucoside and Peonidin 3-Glucoside Inhibit Tumor Cell Growth and Induce Apoptosis In Vitro and Suppress Tumor Growth In Vivo. Nutrition and Cancer, 53, 232-243 https://doi.org/10.1207/s15327914nc5302_12
 
Chiu Chiu-Hsia, Ni Kuang-Huei, Guu Yuan-Kuang, Pan Tzu-Ming (2006): Production of red mold rice using a modified Nagata type koji maker. Applied Microbiology and Biotechnology, 73, 297-304 https://doi.org/10.1007/s00253-006-0457-8
 
Chung C.C., Huang T.C., Chen H.H. (2009): The optimization of Monascus fermentation process for pigments increment and citrinin reduction. In: Bioinformatics and Bioengineering, 2009 IEEE International Conference, June 22–24, 2009, Taichung, Taiwan: 77–83.
 
European Commission (2014): Commission Regulation (EU) No 212/2014 of 6 March 2014 amending Regulation (EC) No 1881/2006 as regards maximum levels of the contaminant citrinin in food supplements based on rice fermented with red yeast Monascus purpureus. Available at http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=OJ:L:2014:067:TOC (accessed Oct 3, 2016).
 
FABRE C. E., SANTERRE A. L., LORET M. O., BABERIAN R., PAREILLEUX A., GOMA G., BLANC P.J. (1993): Production and Food Applications of the Red Pigments of Monascus ruber. Journal of Food Science, 58, 1099-1102 https://doi.org/10.1111/j.1365-2621.1993.tb06123.x
 
Feng Yanli, Shao Yanchun, Zhou Youxiang, Chen Fusheng (2014): Monacolin K production by citrinin-free Monascus pilosus MS-1 and fermentation process monitoring. Engineering in Life Sciences, 14, 538-545 https://doi.org/10.1002/elsc.201300128
 
Fernando Binosha (2013): Rice as a Source of Fibre. Rice Research: Open Access, 1, - https://doi.org/10.4172/jrr.1000e101
 
Journoud Mélanie, Jones Peter J.H (2004): Red yeast rice: a new hypolipidemic drug. Life Sciences, 74, 2675-2683 https://doi.org/10.1016/j.lfs.2003.10.018
 
Kalaivani M., Rajasekaran A. (2014): Improvement of monacolin K/citrinin production ratio in Monascus purpureus using UV mutagenesis. Nutrafoods, 13, 79-84 https://doi.org/10.1007/s13749-014-0021-6
 
Le Bloc’h J., Pauquai T., Bourges C. (2015): Authorised EU health claim for red yeast rice. In: Sadler M. (ed.): Foods, Nutrients and Food Ingredients with Authorised EU Health Claims: Volume 2. Elsevier B.V.: 139–142.
 
Lin Yii-Lih, Wang Teng-Hsu, Lee Min-Hsiung, Su Nan-Wei (2008): Biologically active components and nutraceuticals in the Monascus-fermented rice: a review. Applied Microbiology and Biotechnology, 77, 965-973 https://doi.org/10.1007/s00253-007-1256-6
 
Mienda B.S., Idi A., Umar A. (2011): Microbiological features of solid state fermentation and its applications – an overview. Research in Biotechnology, 2: 21–26.
 
Nimnoi Pongrawee, Lumyong Saisamorn (2011): Improving Solid-State Fermentation of Monascus purpureus on Agricultural Products for Pigment Production. Food and Bioprocess Technology, 4, 1384-1390 https://doi.org/10.1007/s11947-009-0233-8
 
Oh Chan-Ho, Oh Suk-Heung (2004): Effects of Germinated Brown Rice Extracts with Enhanced Levels of GABA on Cancer Cell Proliferation and Apoptosis. Journal of Medicinal Food, 7, 19-23 https://doi.org/10.1089/109662004322984653
 
Panlasigui >Leonora N., Thompson Lilian U. (2009): Blood glucose lowering effects of brown rice in normal and diabetic subjects. International Journal of Food Sciences and Nutrition, 57, 151-158 https://doi.org/10.1080/09637480500410879
 
Park Ji-Young, Han Sang-Ik, Seo Woo Duck, Ra Ji-Eun, Sim Eun-Yeong, Nam Min-Hee (2014): Study on Monascus Strains and Characteristic for Manufacturing Red Yeast Rice with High Production of Monacolin K. Korean Journal of Crop Science, 59, 167-173 https://doi.org/10.7740/kjcs.2014.59.2.167
 
Patil Swati Bhauso, Khan Md. Khalid (2011): Germinated brown rice as a value added rice product: A review. Journal of Food Science and Technology, 48, 661-667 https://doi.org/10.1007/s13197-011-0232-4
 
Rajasekaran Aiyalu, Kalaivani Muthusamy (2012): Biofortification of Indian rice (IR-532-E-576) with monacolin K by RSM optimisation using Monascus purpureus MTCC 1090. Nutrafoods, 11, 49-54 https://doi.org/10.1007/s13749-012-0031-1
 
Shi Yeu-Ching, Pan Tzu-Ming (2011): Beneficial effects of Monascus purpureus NTU 568-fermented products: a review. Applied Microbiology and Biotechnology, 90, 1207-1217 https://doi.org/10.1007/s00253-011-3202-x
 
Songsermsakul P. (2015): Mycotoxins contamination of food in Thailand (2000–2010): Food safety concerns for the world food exporter. International Food Research Journal, 22: 426–434.
 
Su Yuan-Chi, Wang Jyh-Jye, Lin Tzu-Tsen, Pan Tzu-Ming (2003): Production of the secondary metabolites γ-aminobutyric acid and monacolin K by Monascus. Journal of Industrial Microbiology & Biotechnology, 30, 41-46 https://doi.org/10.1007/s10295-002-0001-5
 
Subsaendee T., Kitpreechavanich V., Yongsmith B. (2014): Growth, glucoamylase, pigments and monacolin K production on rice solid culture in flask and koji chamber using Monascus sp. KB9. Chiang Mai Journal of Science, 41: 1044–1057.
 
Tsukahara Masatoshi, Shinzato Naoya, Tamaki Yasutomo, Namihira Tomoyuki, Matsui Toru (2009): Red Yeast Rice Fermentation by Selected Monascus sp. with Deep-Red Color, Lovastatin Production but No Citrinin, and Effect of Temperature-Shift Cultivation on Lovastatin Production. Applied Biochemistry and Biotechnology, 158, 476-482 https://doi.org/10.1007/s12010-009-8553-8
 
Velmurugan Palanivel, Hur Hyun, Balachandar Vellingiri, Kamala-Kannan Seralathan, Lee Kui-Jae, Lee Sang-Myung, Chae Jong-Chan, Shea Patrick J., Oh Byung-Taek (2011): Monascus pigment production by solid-state fermentation with corn cob substrate. Journal of Bioscience and Bioengineering, 112, 590-594 https://doi.org/10.1016/j.jbiosc.2011.08.009
 
Vidyalakshmi R., Paranthaman R., Murugesh S., Singaravadivel K. (2009): Stimulation of Monascus pigments by intervention of different nitrogen sources. Journal of Biotechnology and Biochemistry, 4: 25–28.
 
Wang Jyh-Jye, Lee Chung-Lin, Pan Tzu-Ming (2004): Modified Mutation Method for Screening Low Citrinin-Producing Strains of Monascus purpureus on Rice Culture. Journal of Agricultural and Food Chemistry, 52, 6977-6982 https://doi.org/10.1021/jf049783o
 
Xu Bao-Jun, Wang Qi-Jun, Jia Xiao-Qin, Sung Chang-Keun (2005): Enhanced lovastatin production by solid state fermentation ofMonascus ruber. Biotechnology and Bioprocess Engineering, 10, 78-84 https://doi.org/10.1007/BF02931187
 
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