rocF affects the production of tetramethylpyrazine in fermented soybeans with Bacillus subtilis BJ3-2
Tóm tắt
Tetramethylpyrazine (TTMP) is a flavoring additive that significantly contributes to the formation of flavor compounds in soybean-based fermented foods. Over recent years, the application of TTMP in the food industry and medicine has been widely investigated. In addition, several methods for the industrial-scale production of TTMP, including chemical and biological synthesis, have been proposed. However, there have been few reports on the synthesis of TTMP through amino acid metabolic flux. In this study, we investigated genetic alterations of arginine metabolic flux in solid-state fermentation (SSF) of soybeans with Bacillus subtilis (B.subtilis) BJ3-2 to enhance the TTMP yield.
SSF of soybeans with BJ3-2 exhibited a strong Chi-flavour (a special flavour of ammonia-containing smelly distinct from natto) at 37 °C and a prominent soy sauce-like aroma at 45 °C. Transcriptome sequencing and RT-qPCR verification showed that the rocF gene was highly expressed at 45 °C but not at 37 °C. Moreover, the fermented soybeans with BJ3-2ΔrocF (a rocF knockout strain in B. subtilis BJ3-2 were obtained by homologous recombination) at 45 °C for 72 h displayed a lighter color and a slightly decreased pH, while exhibiting a higher arginine content (increased by 14%) than that of BJ3-2. However, the ammonia content of fermented soybeans with BJ3-2ΔrocF was 43% lower than that of BJ3-2. Inversely, the NH4+ content in fermented soybeans with BJ3-2ΔrocF was increased by 28% (0.410 mg/kg). Notably, the TTMP content in fermented soybeans with BJ3-2ΔrocF and BJ3-2ΔrocF + Arg (treated with 0.05% arginine) were significantly increased by 8.6% (0.4617 mg/g) and 18.58% (0.504 mg/g) respectively than that of the BJ3-2. The present study provides valuable information for understanding the underlying mechanism during the TTMP formation process through arginine metabolic flux.
Tài liệu tham khảo
Xiao ZJ, Xie NZ, Liu PH, Hua DL, Xu P. Tetramethylpyrazine production from glucose by a newly isolated Bacillus mutant. Appl Microbiol Biotechnol. 2006. https://doi.org/10.1007/s00253-006-0491-6.
Müller R, Rappert S. Pyrazines: occurrence, formation and biodegradation. Appl Microbiol Biotechnol. 2010. https://doi.org/10.1007/s00253-009-2362-4.
Fan WL, Yan X, Zhang YH. Characterization of pyrazines in some Chinese liquors and their approximate concentrations. J Agric Food Chem. 2007;55(24):9956–62. https://doi.org/10.1021/jf071357q.
Xiao ZB, Dai SP, Niu YW, Yu HY, Zhu JC, Tian HX, Gu YB. Discrimination of Chinese vinegars based on headspace Solid-Phase Microextraction-Gas chromatography mass spectrometry of volatile compounds and multivariate analysis. J Food Sci. 2011. https://doi.org/10.1111/j.1750-3841.
Meng W, Wang RM, Xiao DG. Metabolic engineering of Bacillus subtilis to enhance the production of tetramethylpyrazine. Biotechnol Lett. 2015. https://doi.org/10.1007/s10529-015-1950-x.
Xu Y, Jiang YF, Li XT, Sun BG, Teng C, Yang R, Xiong K, Fan GS, Wang WH. Systematic characterization of the metabolism of acetoin and its derivative ligustrazine in Bacillus subtilis under micro-Oxygen conditions. J Agric Food Chem. 2018. https://doi.org/10.1021/acs.jafc.8b00113.
Meng W, Xiao DG, Wang RM. Enhanced production of tetramethylpyrazine in Bacillus licheniformis BL1 by bdhA disruption and 2,3-butanediol supplementation. World J Microbiol Biotechnol. 2016. https://doi.org/10.1007/s11274-015-1992-1.
Wang YF, Zhang XJ, Xu CJ, Zhang GX. Synthesis and biological evaluation of danshensu and tetramethylpyrazine conjugates as cardioprotective agents. Chem Pharm Bull (Tokyo). 2017. https://doi.org/10.1248/cpb.c16-00839.
Fadel HHM, Lotfy SN, Asker MMS, Mahmoud MG, Al-Okbi Y. Nutty-like flavor production by Corynbacterium glutamicum1220T from enzymatic soybean hydrolysate. Effect of encapsulation and storage on the nutty flavoring quality. J Adv Res. 2018. https://doi.org/10.1016/j.jare.2018.01.003.
Zhu BF, Xu Y, Fan WL, Wu Q. High-yield fermentative preparation of tetramethylpyrazine by Bacillus sp. using an endogenous precursor approach. J Ind Microbiol Biotechnol. 2010. https://doi.org/10.1007/s10295-009-0661-5.
Wang M, Qin HL, Leng J, Zafar A, Amjad MW, Raja MAG, Hussain MA, Bukhari SNA. Synthesis and biological evaluation of new tetramethylpyrazine based chalcone derivatives as potential anti-alzheimer agents. Chem Biol Drug Des. 2018. https://doi.org/10.1111/cbdd.13355.
Rajini KS, Aparna P, Sasikala C, Ramana CV. Microbial metabolism of pyrazines. Crit Rev Microbiol. 2011. https://doi.org/10.3109/1040841X.2010.512267.
Wang J, Zhong QP, Yang YY, Li HR, Wang L, Tong YG, Fang X, Liao ZL. Comparison of bacterial diversity between two traditional starters and the round-koji-maker starter for traditional cantonese Chi-flavor liquor brewing. Front Microbiol. 2019. https://doi.org/10.3389/fmicb.2018.01053.
Kosuge T, Adachi T, Kamiya H. Isolation of tetramethylpyrazine from culture of Bacillus natto, and biosynthetic pathways of tetramethylpyrazine. Nature. 1962. https://doi.org/10.1038/1951103a0.
Besson I, Creuly C, Gros JB, Larroche C. Pyrazine production by Bacillus subtilis in solid-state fermentation on soybeans. Appl Microbiol Biotechnol. 1997. https://doi.org/10.1007/s002530050961.
Larroche C, Gros JB. Special transformation processes using fungal spores and immobilized cells. Adv Biochem Eng Biotechnol. 1997. https://doi.org/10.1007/BFb0102066.
Larroche C, Besson I, Gros JB. High pyrazine production by Bacillus subtilis in solid substrate fermentation on ground soybeans. Process Biochem. 1999. https://doi.org/10.1016/S0032-9592(98)00141-1.
Zhang JJ, Zhao XY, Zhang JX, Zhao C, Liu JJ, Tian YJ, Yang LP. Effect of deletion of 2,3-butanediol dehydrogenase gene (bdhA) on acetoin production of Bacillus subtilis. Prep Biochem Biotechnol. 2017. https://doi.org/10.1080/10826068.2017.1320293.
Cui DY, Wei YN, Lin LC, Chen SJ, Feng PP, Xiao DG, Lin X, Zhang CY. Increasing yield of 2,3,5,6-Tetramethylpyrazine in Baijiu through Saccharomyces cerevisiae metabolic engineering. Front Microbiol. 2020. https://doi.org/10.3389/fmicb.2020.596306.
Xiao Z, Hou X, Lyu X, Xi L, Zhao JY. Accelerated green process of tetramethylpyrazine production from glucose and diammonium phosphate. Biotechnol Biofuels. 2014. https://doi.org/10.1186/1754-6834-7-106.
Xiao ZJ, Lu JR. Generation of acetoin and its derivatives in foods. J Agric Food Chem. 2014. https://doi.org/10.1021/jf5013902.
Xu YQ, Chu HP, Gao C, Tao F, Zhou ZK, Li K, Li LX, Ma CQ, Xu P. Systematic metabolic engineering of Escherichia coli for high-yield production of fuel bio-chemical 2,3-butanediol. Metab Eng. 2014. https://doi.org/10.1016/j.ymben.
Zhao GZ, Feng YX, Hadiatullah H, Zheng FP, Yao YP. Chemical characteristics of three kinds of Japanese soy sauce based on electronic senses and GC-MS analyses. Front Microbiol. 2021. https://doi.org/10.3389/fmicb.2020.579808.
Wen AY, Qin LK, Zeng HY, Zhu Y. Comprehensive evaluation of physicochemical properties and antioxidant activity of B. subtilis-fermented polished adlay subjected to different drying methods. Food Sci Nutr. 2020. https://doi.org/10.1002/fsn3.1508.
Hampel A, Huber C, Geffers R, Spona-Friedl M, Eisenreich W, Bange FC. Mycobacterium tuberculosis is a natural ornithine aminotransferase (rocD) mutant and depends on Rv2323c for growth on arginine. PLoS ONE. 2015. https://doi.org/10.1371/journal.pone.0136914.
Lu CD. Pathways and regulation of bacterial arginine metabolism and perspectives for obtaining arginine overproducing strains. Appl Microbiol Biotechnol. 2006. https://doi.org/10.1007/s00253-005-0308-z.
Li WX, Zhou XX, Lu P. Bottlenecks in the expression and secretion of heterologous proteins in Bacillus subtilis. Res Microbiol. 2004. https://doi.org/10.1016/j.resmic.2004.05.002.
Yan Z, Zheng XW, Chen JY, Han JS, Han BZ. Effect of different Bacillus strains on the profile of organic acids in a liquid culture of Daqu. Asymmetric Michael Add Alanine Deriv. 2013. https://doi.org/10.1002/jib.58.
Jia DX, Wu YJ. Screening and Identification of Bacillus for lobster sauce fermentation. Food Sci. 2009. https://doi.org/10.3321/j.issn:1002-6630.2009.05.051.
Ralli P, Srivastava AC, O’Donovan G. Regulation of the pyrimidine biosynthetic pathway in a pyrD knockout mutant of Pseudomonas aeruginosa. J Basic Microbiol. 2010. https://doi.org/10.1002/jobm.200610248.
Butcher BG, Chakravarthy S, D’Amico K, Stoos KB, Filiatrault MJ. Disruption of the carA gene in Pseudomonas syringae results in reduced fitness and alters motility. BMC Microbiol. 2016. https://doi.org/10.1186/s12866-016-0819-z.
Yang HJ, Bogomolnaya L, McClelland M, Andrews-Polymenis H. De novo pyrimidine synthesis is necessary for intestinal colonization of Salmonella Typhimurium in chicks. PLoS ONE. 2017. https://doi.org/10.1371/journal.pone.0183751.
Shen YF. Type of flavor of Baijiu. Niangjiu. 2003. CNKI:SUN:NJZZ.0.2003–01–000.
Liu HX, Qu XX, Zhao SM, Lu ZX, Zhang C, Bie XM. Characterization of a Bacillus subtilis surfactin synthetase knockout and antimicrobial activity analysis. J Biotechnol. 2016. https://doi.org/10.1016/j.jbiotec.2016.08.018.
Jalbout AF, Shipar MAH, Trzaskowski B, Adamowicz. Formation of pyrazines in hydroxyacetaldehyde and glycine nonenzymatic browning Maillard reaction: a computational study. Food Chem. 2007. https://doi.org/10.1016/j.foodchem.2006.07.061.
Li ZP, Ma DX, He YY, Guo SQ, Liu FG, Liu XB. Simultaneous ultrasound and heat enhance functional properties of glycosylated lactoferrin. Molecules. 2020. https://doi.org/10.3390/molecules25235774.
Scaman C, Nakai S, Aminlari M. Effect of pH, temperature and sodium bisulfite or cysteine on the level of Maillard-based conjugation of lysozyme with dextran, galactomannan and mannan. Food Chem. 2006. https://doi.org/10.1016/j.foodchem.2005.08.003.
Benjakul S, Lertittikul W, Bauer F. Antioxidant activity of Maillard reaction products from a porcine plasma protein-sugar model system. Food Chem. 2005. https://doi.org/10.1016/j.foodchem.2004.10.019.
Chen SL, Jin SY, Chen CS. Relative reactivities of glucose and galactose in browning and pyruvaldehyde formation in sugar/glycine model systems. Food Chem. 2005. https://doi.org/10.1016/j.foodchem.2004.09.005.
Ramírez-Jiménez A, García-Villanova B, Guerra-Hernández E. Effect of toasting time on the browning of sliced bread. J Sci Food Agric. 2001. https://doi.org/10.1002/jsfa.840.
Liu PL, Lu XM, Li NY, Zheng ZJ, Qiao XG. Characterization, variables, and antioxidant activity of the Maillard reaction in a Fructose-Histidine model system. Molecules. 2018. https://doi.org/10.3390/molecules24010056.
Kanamori T, Kanou N, Atomi H, Imanaka T. Enzymatic characterization of a prokaryotic urea carboxylase. J Bacteriol. 2004. https://doi.org/10.1128/JB.186.9.2532-2539.2004.
Kanehisa M, Furumichi M, Sato Y, Ishiguro-Watanabe M, Tanabe. KEGG: integrating viruses and cellular organisms. Nucl Acids Res. 2021. https://doi.org/10.1093/nar/gkaa970.
Zhang LC, Zhu MK, Ren LJ, Li AZ, Chen GP, Hu ZL. The SlFSR gene controls fruit shelf-life in tomato. J Exp Bot. 2018. https://doi.org/10.1093/jxb/ery116.
Zhang XZ, Cui ZL, Hong Q, Li SP. High-level expression and secretion of methyl parathion hydrolase in Bacillus subtilis WB800. Appl Environ Microbiol. 2005. https://doi.org/10.1128/AEM.71.7.4101-4103.2005.
Phan TT, Nguyen HD, Schumann W. Novel plasmid-based expression vectors for intra-and extracellular production of recombinant proteins in Bacillus subtilis. Protein Expr Purif. 2006;46:189–95. https://doi.org/10.1016/j.pep.2005.07.005.
Xu W, Xu Q, Chen JH, Lu ZM, Xia R, Li GQ, Xu ZH, Ma YH. Ligustrazine formation in Zhenjiang aromatic vinegar: changes during fermentation and storing process. J Sci Food Agric. 2011. https://doi.org/10.1002/jsfa.4356.
Favaro G, Pastore P, Saccani G, Cavalli S. Determination of biogenic amines in fresh and processed meat by ion chromatography and integrated pulsed amperometric detection on Au electrode. Food Chem. 2007. https://doi.org/10.1016/j.foodchem.2007.04.071.