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Effects of NADH Availability on 3-Phenyllactic Acid Production by Lactobacillus plantarum Expressing Formate Dehydrogenase

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Abstract

It is well known that cofactors play a key role in the production of different compounds in bioconversion processes, while the high cost of cofactors limits their usage in industrial applications. In the present study, a NADH regeneration system was successfully developed in Lactobacillus plantarum by expressing the fdh gene coding for formate dehydrogenase (FDH) from Candida boidinii. Results indicated that the FDH was expressed with the highest activity of 0.82 U/mg of protein when cells entered early stationary phase. In addition, the expression of FDH increased the intracellular level of NADH and NADH/NAD+ ratio in L. plantarum, and therefore, enhanced the NADH-dependent production of 3-phenyllactic acid (PLA) in repeated and fed-batch bioconversions. In brief, the results demonstrate that the NADH regeneration by expressing FDH is a promising strategy for producing NADH-dependent microbial metabolites in L. plantarum.

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References

  1. Mu WM, Yu SH, Zhu LJ, Zhang T, Jiang B (2012) Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound. Appl Microbiol Biotechnol 95(5):1155–1163

    Article  CAS  PubMed  Google Scholar 

  2. Zheng ZJ, Ma CQ, Gao C, Li FS, Qin JY, Zhang HW, Wang K, Xu P (2011) Efficient conversion of phenylpyruvic acid to phenyllactic acid by using whole cells of Bacillus coagulans SDM. PLoS ONE 6:e19030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Vermeulen N, Ganzle MG, Vogel RF (2006) Influence of peptide supply and cosubstrates on phenylalanine metabolism of Lactobacillus sanfranciscensis DSM20451(T) and Lactobacillus plantarum TMW1.468. J Agric Food Chem 54:3832–3839

    Article  CAS  PubMed  Google Scholar 

  4. Li XF, Jiang B, Pan BL (2007) Biotransformation of phenylpyruvic acid to phenyllactic acid by growing and resting cells of a Lactobacillus sp. Biotechnol Lett 29:593–597

    Article  CAS  PubMed  Google Scholar 

  5. Valerio F, Di Biase M, Lattanzio VMT, Lavermicocca P (2016) Improvement of the antifungal activity of lactic acid bacteria by addition to the growth medium of phenylpyruvic acid, a precursor of phenyllactic acid. Int J Food Microbiol 222:2221–2227

    Article  CAS  Google Scholar 

  6. Li L, Shin SY, Lee KW, Han NS (2014) Production of natural antimicrobial compound d-phenyllactic acid using Leuconostoc mesenteroides ATCC 8293 whole cells involving highly active d-lactate dehydrogenase. Lett Appl Microbiol 59:404–411

    Article  CAS  PubMed  Google Scholar 

  7. Mu WM, Chen C, Li XF, Zhang T, Jiang B (2009) Optimization of culture medium for the production of phenyllactic acid by Lactobacillus sp. SK007. Bioresour Technol 100(3):1366–1370

    Article  CAS  PubMed  Google Scholar 

  8. Mu WM, Liu FL, Jia JH, Chen C, Zhang T, Jiang B (2009) 3-Phenyllactic acid production by substrate feeding and pH-control in fed-batch fermentation of Lactobacillus sp. SK007. Bioresour Technol 100(21):5226–5229

    Article  CAS  PubMed  Google Scholar 

  9. Rodríguez N, Salgado JM, Cortés S, Domínguez JM (2012) Antimicrobial activity of d-3-phenyllactic acid produced by fed-batch process against Salmonella enterica. Food Control 25(1):274–284

    Article  CAS  Google Scholar 

  10. Stephanopoulos G (1999) Metabolic fluxes and metabolic engineering. Metab Eng 1(1):1–11

    Article  CAS  Google Scholar 

  11. San KY, Bennett GN, Berríos-Rivera SJ, Vadali RV, Yang YT, Horton E, Rudolph FB, Sariyar B, Blackwood K (2002) Metabolic engineering through cofactor manipulation and its effects on metabolic flux redistribution in Escherichia coli. Metab Eng 4:182–192

    Article  CAS  PubMed  Google Scholar 

  12. Foster JW, Park YK, Penfound T, Fenger T, Spector MP (1990) Regulation of NAD metabolism in Salmonella typhimurium: molecular sequence analysis of the bifunctional nadR regulator and the nadA-pnuC operon. J Bacteriol 172:4187–4196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ma Z, Shentu XP, Bian YL, Yu XP (2013) Effects of NADH availability on the Klebsiella pneumonia strain with 1,3-propanediol operon over-expression. J Basic Microbiol 53:348–354

    Article  CAS  Google Scholar 

  14. Li XF, Jiang B, Pan BL, Mu WM, Zhang T (2008) Purification and partial characterization of Lactobacillus species SK007 lactate dehydrogenase (LDH) catalyzing phenylpyruvic acid (PPA) conversion into phenyllactic acid (PLA). J Agric Food Chem 56(7):2392–2399

    Article  CAS  PubMed  Google Scholar 

  15. Kaup B, Bringer-Meyer S, Sahm H (2004) Metabolic engineering of Escherichia coli: construction of an efficient biocatalyst for d-mannitol formation in a whole-cell biotransformation. Appl Microbiol Biotechnol 64:333–339

    Article  CAS  PubMed  Google Scholar 

  16. Zhang Y, Huang Z, Du C, Li Y, Cao Z (2009) Introduction of an NADH regeneration system into Klebsiella oxytoca leads to an enhanced oxidative and reductive metabolism of glycerol. Metab Eng 11:101–106

    Article  CAS  PubMed  Google Scholar 

  17. Xu GC, Zhang LL, Ni Y (2016) Enzymatic preparation of d-phenyllactic acid at high space-time yield with a novel phenylpyruvate reductase identified from Lactobacillus sp. J Biotechnol 222:29–37

    Article  CAS  PubMed  Google Scholar 

  18. Lin SS, Miyawaki O, Nakamura K (1999) Continuous production of l-carnitine with NADH regeneration by a nanofiltration membrane reactor with coimmobilized l-carnitine dehydrogenase and glucose dehydrogenase. J Biosci Bioeng 87(3):361–364

    Article  CAS  PubMed  Google Scholar 

  19. Wang Y, Li LX, Ma CQ, Gao C, Tao F, Xu P (2013) Engineering of cofactor regeneration enhances (2S,3S)-2,3-butanediol production from diacetyl. Sci Rep 3:2643

    Article  PubMed  PubMed Central  Google Scholar 

  20. Berrios-Rivera SJ, Bennett GN, San KY (2002) Metabolic engineering of Escherichia coli: increase of NADH availability by expressing an NAD+-dependent formate dehydrogenase. Metab Eng 4:217–229

    Article  CAS  PubMed  Google Scholar 

  21. Kratzer R, Pukl M, Egger S, Nidetzky B (2008) Whole-cell bioreduction of aromatic α-keto esters using Candida tenuis xylose reductase and Candida boidinii formate dehydrogenase co-expressed in Escherichia coli. Microb Cell Fact 7:37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Liu WM, Ma HM, Luo JX, Shen WH, Xu X, Li S, Hu Y, Huang H (2004) Efficient synthesis of l-tert-leucine through reductive amination using leucine dehydrogenase and formate dehydrogenase coexpressed in recombinant E. coli. Biochem Eng J 91:204–209

    Article  CAS  Google Scholar 

  23. Van de Guchte M, Van der Vossen JM, Kok J, Venema G (1989) Construction of a Lactococcal expression vector: expression of hen egg white lysozyme in Lactococcus lactis subsp. lactis. Appl Environ Microbiol 55(1):224–228

    PubMed  PubMed Central  Google Scholar 

  24. Kolandaswamy A, George L, Sadasivam S (2009) Heterologous expression of oxalate decarboxylase in Lactobacillus plantarum NC8. Curr Microbiol 58:117–121

    Article  CAS  PubMed  Google Scholar 

  25. Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  26. Cheng X, Liu F, Zhang YX, Jiang YS (2013) Cloning and expression of a urate oxidase and creatinine hydrolase fusion gene in Escherichia coli. Ren Fail 35(2):275–278

    Article  CAS  PubMed  Google Scholar 

  27. Mnisi SM (2006) Cloning, properties and expression of a novel esterase from Bacillus coagulans strain 18-11. Dissertation, University of Pretoria

  28. Brurberg MB, Haandrikman AJ, Leenhouts KJ, Venema G, Nes IF (1994) Expression of a chitinase gene from Serratia marcescens in Lactococcus lactis and Lactobacillus plantarum. Appl Microbiol Biotechnol 42(1):108–115

    Article  CAS  PubMed  Google Scholar 

  29. Miao YZ, Xu H, Fei BJ, Qiao DR, Cao Y (2013) Expression of food-grade phytase in Lactococcus lactis from optimized conditions in milk broth. J Biosci Bioeng 116(1):34–38

    Article  CAS  PubMed  Google Scholar 

  30. Ji XJ, Xia ZF, Fu NH, Nie ZK, Shen MQ, Tian QQ, Huang H (2013) Cofactor engineering through heterologous expression of an NADH oxidase and its impact on metabolic flux redistribution in Klebsiella pneumonia. Biotechnol Biofuels 6:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Li N, Wang YL, Zhu P, Liu ZM, Guo BH, Ren J (2015) Improvement of exopolysaccharide production in Lactobacillus casei LC2W by expression of NADH oxidase gene. Microbiol Res 171:73–77

    Article  CAS  PubMed  Google Scholar 

  32. Zheng ZJ, Zhao MY, Zang Y, Zhou Y, Ouyang J (2015) Production of optically pure-phenyllactic acid by using engineered Escherichia coli coexpressing l-lactate dehydrogenase and formate dehydrogenase. J Biotechnol 207:47–51

    Article  CAS  PubMed  Google Scholar 

  33. Yu SH, Zhu LJ, Zhou C, An T, Jiang B, Mu WM (2014) Enzymatic production of d-3-phenyllactic acid by Pediococcus pentosaceus d-lactate dehydrogenase with NADH regeneration by Ogataea parapolymorpha formate dehydrogenase. Biotechnol Lett 36:627–631

    Article  CAS  PubMed  Google Scholar 

  34. Jia JH, Mu WM, Zhang T, Jiang B (2010) Bioconversion of phenylpyruvate to phenyllactate, gene cloning, expression, and enzymatic characterization of d- and l1-lactate dehydrogenase from Lactobacillus plantarum SK002. Appl Biochem Biotechnol 162(1):242–251

    Article  CAS  PubMed  Google Scholar 

  35. Reed MC, Lieb A, Nijhout HF (2010) The biological significance of substrate inhibition: a mechanism with diverse functions. BioEssays 32:422–429

    Article  CAS  PubMed  Google Scholar 

  36. Lin SKC, Du CY, Koutinas A, Wang RH, Webb C (2008) Substrate and product inhibition kinetics in succinic acid production by Actinobacillus succinogenes. Biochem Eng J 41(2):128–135

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by Natural Science Foundation of the Higher Education Institutions of Jiangsu Province (Grant no. 16KJB180033).

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Correspondence to Minghua Li.

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Li, M., Meng, X., Sun, Z. et al. Effects of NADH Availability on 3-Phenyllactic Acid Production by Lactobacillus plantarum Expressing Formate Dehydrogenase. Curr Microbiol 76, 706–712 (2019). https://doi.org/10.1007/s00284-019-01681-0

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  • DOI: https://doi.org/10.1007/s00284-019-01681-0

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