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Effects of pigment and citrinin biosynthesis on the metabolism and morphology of Monascus purpureus in submerged fermentation

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Abstract

The effects of the secondary metabolite biosynthesis on the metabolism and morphology of the Monascus purpureus were investigated in this study. Hypha and septum length became longer after deletion of genes pigR and pksCT in M. purpureus LQ-6 by Agrobacterium tumefaciens-mediated transformation technology, highly branched hyphae, much smaller and freely dispersed mycelial pellets were observed in M. purpureus. Compared with that in the wild-type, the level of intracellular NADH and NADPH was almost constant in M. purpureus ΔpigR at 4 days, but the NADH and NADPH levels decreased by 1.58-fold and 3.71-fold in M. purpureus ΔpksCT. The present study can not only provide a kind of strategy to improve the Monascus pigments production, but also provide theoretical support for the further study of relationship between the secondary metabolites, metabolism and morphological change.

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References

  • Balakrishnan B, Karki S, Chiu SH, Kim HJ, Suh JW, Nam B, Yoon YM, Chen CC, Kwon HJ. Genetic localization and in vivo characterization of a Monascus azaphilone pigment biosynthetic gene cluster. Appl. Microbiol. Biotechnol. 97: 6337-6345 (2013)

    Article  CAS  PubMed  Google Scholar 

  • Chen YP, Tseng CP, Chien IL, Wang WY, Liaw LL, Yuan GF. Exploring the distribution of citrinin biosynthesis related genes among Monascus species. J. Agric. Food Chem. 56: 11767-11772 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Bei Q, Huang T, Wu ZQ. Tracking of pigment accumulation and secretion in extractive fermentation of Monascus anka GIM 3.592. Microb. Cell Fact. 16: 172 (2017)

    Article  Google Scholar 

  • Chen G, Wang MH, Tian XF, Wu ZQ. Analyses of Monascus pigment secretion and cellular morphology in non-ionic surfactant micelle aqueous solution. Microb. Biotechnol. 11: 409-419 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Fu GM, Xu Y, Li YP, Tan WH. Construction of a replacement vector to disrupt pksCT gene for the mycotoxin citrinin biosynthesis in Monascus aurantiacus and maintain food red pigment production. Asia Pac. J. Clin. Nutr. 16 Suppl 1: 137-142 (2007)

    CAS  PubMed  Google Scholar 

  • Hajjaj H, Klaébé A, Loret MO, Goma G, Blanc P, Francois JM. Biosynthetic pathway of citrinin in the filamentous fungus Monascus ruber as revealed by 13C nuclear magnetic resonance. Appl. Environ. Microb. 65: 311-314 (1999)

    Article  CAS  Google Scholar 

  • Hu ZQ, Zhang XH, Wu ZQ, Qi HS, Wang ZL. Export of intracellular Monascus pigments by two-stage microbial fermentation in nonionic surfactant micelle aqueous solution. J. Biotechnol. 162: 202-209 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Huang T, Tan HL, Lu FJ, Chen G, Wu ZQ. Changing oxidoreduction potential to improve water-soluble yellow pigment production with Monascus ruber CGMCC 10910. Microb. Cell Fact. 16: 208 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Ibrahim D. Effect of agitation speed on the morphology of Aspergillus nigerHFD5A-1 hyphae and its pectinase production in submerged fermentation. World J. Biol. Chem. 6: 265 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Jia XQ, Xu ZN, Zhou LP, Sung CK. Elimination of the mycotoxin citrinin production in the industrial important strain Monascus purpureus SM001. Metab. Eng. 12: 1-7 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Ku S. Beneficial effects of Monascus sp. KCCM 10093 pigments and derivatives: A mini review. Molecules. 23:98 (2018)

    Article  PubMed Central  Google Scholar 

  • Kim HJ, Kim JH, Oh HJ, Shin CS. Morphology control of Monascus cells and scale-up of pigment fermentation. Process Biochem. 38: 649-655 (2002)

    Article  CAS  Google Scholar 

  • Kwon HJ, Balakrishnan B, Kim YK. Some Monascus purpureus genomes lack the Monacolin K biosynthesis locus. J. Appl. Biol. Chem. 59: 45-47 (2016)

    Article  CAS  Google Scholar 

  • Lai Y, Wang L, Qing L, Chen FS. Effects of cyclic AMP on development and secondary metabolites of Monascus ruber M-7. Lett. Appl. Microbiol. 52: 420-426 (2011)

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Ji GE, Lee I. Natural occurring levels of citrinin and Monacolin K in Korean Monascus fermentation products. Food Sci. Biotechnol. 16: 142-145 (2007)

    Google Scholar 

  • Lin L, Wu SF, Li ZJ, Ren ZY, Chen MH, Wang CL. High expression level of mok E enhances the production of Monacolin K in Monascus. Food Biotechnol. 32: 35-46 (2018)

    Article  CAS  Google Scholar 

  • Liu J, Guo T, Luo YC, Chai XY, Wu JY, Zhao W, Jiao PF, Luo FJ, Lin QL. Enhancement of Monascus pigment productivity via a simultaneous fermentation process and separation system using immobilized-cell fermentation. Bioresour. Technol. 272: 552-560 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Lv J, Zhang BB, Liu XD, Zhang C, Chen L, Xu GR, Cheung PCK (2017) Enhanced production of natural yellow pigments from Monascus purpureus by liquid culture: The relationship between fermentation conditions and mycelial morphology. J. Biosci. Bioeng. 124: 452-458

    Article  CAS  PubMed  Google Scholar 

  • Ning ZQ, Cui H, Xu Y, Huang ZB, Tu Z, Li YP(2017) Deleting the citrinin biosynthesis-related gene, ctnE, to greatly reduce citrinin production in Monascus aurantiacus Li AS3.4384. Int. J. Food Microbiol. 241: 325-330

    Article  CAS  PubMed  Google Scholar 

  • Papagianni M. Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol. Adv. 22: 189-259 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Patakova P. Monascus secondary metabolites: production and biological activity. J. Ind. Microbiol. Biot. 40: 169-181 (2013)

    Article  CAS  Google Scholar 

  • Shao YC, Ding YD, Zhao Y, Yang S, Xie BJ, Chen FS. Characteristic analysis of transformants in T-DNA mutation library of Monascus ruber. World J. Microbiol. Biotechnol. 25: 989-995 (2009)

    Article  CAS  Google Scholar 

  • Shao YC, Lei M, Mao ZJ, Zhou YX, Chen FS. Insights into Monascus biology at the genetic level. Appl. Microbiol. Biotechnol. 98: 3911-3922 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T, Kinoshita H, Ishihara S, Sakai K, Nagai S, Nihira T. Polyketide synthase gene responsible for citrinin biosynthesis in Monascus purpureus. Appl. Environ. Microbiol. 71: 3453-3457 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun XW, Wu HF, Zhao GH, Li ZM, Wu XH, Liu H, Zheng ZM. Morphological regulation of Aspergillus niger to improve citric acid production by chsC gene silencing. Bioproc. Biosyst. Eng. 41: 1029-1038 (2018)

    Article  CAS  Google Scholar 

  • Terán HR, de Souza RA, Marcelino PF, da Silva SS, Dragone G, Mussatto SI, Santos JC. Sugarcane bagasse hydrolysate as a potential feedstock for red pigment production by Monascus ruber. Food Chem. 245: 786-791 (2018)

    Article  Google Scholar 

  • Vecht-Lifshitz SE, Magdassi S, Braun S. Pellet formation and cellular aggregation in Streptomyces tendae. Biotechnol. Bioeng. 35: 890-896 (1990)

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Zhang XH, Wu ZQ, Wang ZL. Investigation of relationship between lipid and Monascus pigment accumulation by extractive fermentation. J. Biotechnol. 212: 167-173 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Xie NN, Liu QP, Chen FS. Deletion of pigR gene in Monascus ruber leads to loss of pigment production. Biotechnol. Lett. 35: 1425-1432 (2013)

    Article  CAS  PubMed  Google Scholar 

  • Xie NN, Zhang YP, Chen FS. Identification of a pigment-polyketide synthase gene deleted mutant of Monascus ruber M7. Wei Sheng Wu Xue Bao. 55: 863-872 (2015)

    CAS  PubMed  Google Scholar 

  • Yang XL, Dong Y, Liu GR, Zhang C, Cao YP, Wang CT (2019) Effects of nonionic surfactants on pigment excretion and cell morphology in extractive fermentation of Monascus sp NJ1. J. Sci. Food Agric. 99: 1233-1239

    Article  CAS  PubMed  Google Scholar 

  • Zhang C, Liang J, Yang L, Chai SY, Zhang CX, Sun BG, Wang CT. Glutamic acid promotes monacolin K production and monacolin K biosynthetic gene cluster expression in Monascus. AMB Express. 7: 22 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang K, Yu C, Yang ST. Effects of soybean meal hydrolysate as the nitrogen source on seed culture morphology and fumaric acid production by Rhizopus oryzae. Process Biochem. 50: 173-179 (2015)

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank Prof. Tiangang Liu from Wuhan University, China, for kindly providing the pXS plasmid for cloning selection marker G418 fragment and Prof. Feng Yu from Hunan University, China, for kindly providing A. tumefaciens EHA105.

Funding

This work was supported by National Natural Science Foundation of China (Grant No. 31571874); 2011 Collaborative Innovation Center of Hunan province (2013, No. 448); Natural Science Foundation of Hunan Province (No. 2018JJ3872); Natural Science Foundation of Hunan Province (No. 2018JJ2672); Key Laboratory of Staple Grain Processing, Ministry of Agriculture and Rural Affairs of the People’s Republic of China (No. DZLS201706); Research and Development Plan in Key Areas of Hunan Province (No. 2019NK2111); and Natural Science Foundation of Hunan Province (No. 6082019JJ40542).

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Authors and Affiliations

  1. Key Laboratory of Staple Grain Processing, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Zhengzhou, 450002, Henan, China

    Xueying Chai, Zhilu Ai & Jun Liu

  2. National Engineering Laboratory for Deep Process of Rice and Byproducts, Hunan Key Laboratory of Grain-oil Deep Process and Quality Control, Hunan Key Laboratory of Processed Food for Special Medical Purpose, College of Food Science and Engineering, Central South University of Forestry and Technology, Changsha, 41004, Hunan, China

    Xueying Chai, Jun Liu, Ting Guo, Jingyan Wu, Jie Bai & Qinlu Lin

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  1. Xueying Chai
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  2. Zhilu Ai
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Correspondence to Qinlu Lin.

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Fig. S1

The construction process of the pigR deletion plasmid pCAMBIA3300-ΔpigR (JPEG 99 kb)

Fig. S2

Supplementary material 2 (PDF 50 kb)

Fig. S3

Supplementary material 3 (JPEG 47 kb)

Fig. S4

Supplementary material 4 (JPEG 458 kb)

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Supplementary material 6 (DOCX 17 kb)

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Chai, X., Ai, Z., Liu, J. et al. Effects of pigment and citrinin biosynthesis on the metabolism and morphology of Monascus purpureus in submerged fermentation. Food Sci Biotechnol 29, 927–937 (2020). https://doi.org/10.1007/s10068-020-00745-3

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