Advertisement

Engineering Lactococcus lactis for D-Lactic Acid Production from Starch

  • Yuji AsoEmail author
  • Ayaka Hashimoto
  • Hitomi Ohara
Article

Abstract

Bioprocess development is a current requirement to enhance the global production of D-lactic acid. Herein, we report a new bioprocess for D-lactic acid production directly from starch using engineered Lactococcus lactis NZ9000. To modify L. lactis as a D-lactic acid producer, its major endogenous L-lactate dehydrogenase (L-Ldh) gene was replaced with a heterologous D-Ldh gene from Lactobacillus delbrueckii subsp. lactis JCM 1107. The resulting strain AH1 showed a somewhat slower growth rate but similar lactic acid production compared to those of the intact strain when cultivated with glucose as a carbon source. The chemical purity of D-lactic acid produced by L. lactis AH1 was 93.8%, and the enzymatic activities of D- and L-Ldh in AH1 were 1.54 U/mL and 0.05 U/mL, respectively. Next, a heterologous α-amylase gene from Streptococcus bovis NRIC 1535 cloned into an expression vector pNZ8048 was introduced into AH1. The resulting strain AH2 showed an amylolytic activity of 0.26 U/mL in the culture supernatant. Direct production of D-lactic acid from starch as the carbon source was demonstrated using L. lactis AH2, resulting in D-lactic acid production at a concentration of 15.0 g/L after 24 h cultivation. To our knowledge, this is the first report on D-lactic acid production in engineered L. lactis.

Notes

Acknowledgements

We thank the NIZO Food Research (Netherlands) for providing us with L. lactis NZ9000 and pNZ8048. We also thank NODAI Culture Collection Center (Tokyo University of Agriculture, Japan) for providing us with S. bovis NRIC 1535. This work was supported by JSPS KAKENHI Grant Number 24580110.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest for this study.

References

  1. 1.
    Rathin D, Henry M (2006) Lactic acid: recent advances in products, processes and technologies—a review. J Chem Technol Biotechnol 81:1119–1129CrossRefGoogle Scholar
  2. 2.
    Litchfield JH (2009) Lactic acid, microbially produced. In: Schaechter MO (ed) Encyclopedia of microbiology. Oxford Academic Press, Oxford, pp 362–372CrossRefGoogle Scholar
  3. 3.
    Martinez FAC, Balciunas EM, Salgado JM, González JMD, Converti A, de Souza Oliveira RP (2013) Lactic acid properties, applications and production: a review. Trends Food Sci Technol 30:70–83CrossRefGoogle Scholar
  4. 4.
    Henton DE, Gruber P, Lunt J, Randall J (2005) Polylactic acid technology. In: Mohanty AK, Misra M, Drzal LT (eds) Natural fibers, biopolymers, and biocomposites. Taylor & Francis, Boca Raton, pp 527–577Google Scholar
  5. 5.
    Garlotta D (2001) A literature review of poly (lactic acid). J Pol Environ 9:63–84CrossRefGoogle Scholar
  6. 6.
    Tsuji H (2005) Poly(lactide) stereocomplexes: formation, structure, properties, degradation, and applications. Macromol Biosci 5:569–597CrossRefGoogle Scholar
  7. 7.
    de Vos S (2008) Improving heat-resistance of PLA using poly(d-lactide). Bioplast Mag 3:21–25Google Scholar
  8. 8.
    Axelsson L (2004) Lactic acid bacteria: classification and physiology. In: Salminen S, Von Wright A (eds) Lactic acid bacteria. Microbiological and functional aspects, 3rd edn. Marcel Dekker, New York, pp 1–72Google Scholar
  9. 9.
    Chao GAO, Cuiqing MA, Ping XU (2011) Biotechnological routes based on lactic acid production from biomass. Biotechnol Adv 29:930–939CrossRefGoogle Scholar
  10. 10.
    Abdel-Rahman MA, Tashiro Y, Sonomoto K (2013) Recent advances in lactic acid production by microbial fermentation processes. Biotechnol Adv 31:877–902CrossRefGoogle Scholar
  11. 11.
    Ghaffar T, Irshad M, Anwar Z, Aqil T, Zulifqar Z, Tariq A, Kamran M, Ehsan N, Mehmood S (2014) Recent trends in lactic acid biotechnology: a brief review on production to purification. J Radiat Res Appl Sci 7:222–229CrossRefGoogle Scholar
  12. 12.
    Eş I, Mousavi Khaneghah A, Barba FJ, Saraiva JA, Sant’Ana AS, Hashemi SMB (2018) Recent advancements in lactic acid production—a review. Food Res Int 107:763–770CrossRefGoogle Scholar
  13. 13.
    Holo H, Nes IF (1989) High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl Environ Microbiol 55:3119–3123Google Scholar
  14. 14.
    McKay LL, Kathleen AB (1990) Applications for biotechnology: present and future improvements in lactic acid bacteria. FEMS Microbiol Rev 7:3–14CrossRefGoogle Scholar
  15. 15.
    van de Guchte M, Kok J, Venema G (1992) Gene expression in Lactococcus lactis. FEMS Microbiol Rev 8:73–92CrossRefGoogle Scholar
  16. 16.
    de Vos WM (1999) Gene expression systems for lactic acid bacteria. Curr Opin Microbiol 2:289–295CrossRefGoogle Scholar
  17. 17.
    Morello E, Bermudez-Humaran LG, Llull D, Sole V, Miraglio N, Langella P, Poquet I (2008) Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion. J Mol Microbiol Biotechnol 14:48–58CrossRefGoogle Scholar
  18. 18.
    de Ruyter PG, Kuipers OP, Beerthuyzen MM, van Alen-Boerrigter I, de Vos WM (1996) Functional analysis of promoters in the nisin gene cluster of Lactococcus lactis. J Bacteriol 178:3434–3439CrossRefGoogle Scholar
  19. 19.
    Mierau I, Kleerebezem M (2005) 10 years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis. Appl Microbiol Biotechnol 68:705–717CrossRefGoogle Scholar
  20. 20.
    Mierau I, Olieman K, Mond J, Smid EJ (2005) Optimization of the Lactococcus lactis nisin-controlled gene expression system NICE for industrial applications. Microbial Cell Fact 4:16CrossRefGoogle Scholar
  21. 21.
    Mierau I, Leij P, Van Swam I, Blommestein B, Floris E, Mond J, Smid EJ (2005) Industrial-scale production and purification of a heterologous protein in Lactococcus lactis using the nisin-controlled gene expression system NICE: the case of lysostaphin. Microbial Cell Fact 4:15CrossRefGoogle Scholar
  22. 22.
    Zink A, Klein JR, Plapp R (1991) Transformation of Lactobacillus delbrueckii ssp. lactis by electroporation and cloning of origins of replication by use of a positive selection vector. FEMS Microbiol Lett 78:207–212Google Scholar
  23. 23.
    Serror P, Sasaki T, Ehrlich SD, Maguin E (2002) Electrotransformation of Lactobacillus delbrueckii subsp. bulgaricus and L. delbrueckii subsp. lactis with various plasmids. Appl Environ Microbiol 68:46–52CrossRefGoogle Scholar
  24. 24.
    Palomino MM, Allievi MC, Prado-Acosta M, Sanchez-Rivas C, Ruzal SM (2010) New method for electroporation of Lactobacillus species grown in high salt. J Microbiol Methods 83:164–167CrossRefGoogle Scholar
  25. 25.
    Zhou S, Shanmugam KT, Ingram LO (2003) Functional replacement of the Escherichia coli d-(-)-lactate dehydrogenase gene (ldhA) with the l-(+)-lactate dehydrogenase gene (ldhL) from Pediococcus acidilactici. Appl Environ Microbiol 69:2237–2344CrossRefGoogle Scholar
  26. 26.
    Aso Y, Tsubaki M, Long BHD, Murakami R, Nagata K, Okano H, Phuong Dung NT, Ohara H (2019) Continuous production of d-lactic acid from cellobiose in cell recycle fermentation using β-glucosidase-displaying Escherichia coli. J Biosci Bioeng 127:441–446CrossRefGoogle Scholar
  27. 27.
    Okano K, Zhang Q, Shinkawa S, Yoshida S, Tanaka T, Fukuda H, Kondo A (2009) Efficient production of optically pure d-lactic acid from raw corn starch by using a genetically modified l-lactate dehydrogenase gene-deficient and α-amylase-secreting Lactobacillus plantarum strain. Appl Environ Microbiol 75:462–467CrossRefGoogle Scholar
  28. 28.
    Narita J, Okano K, Kitao T, Ishida S, Sewaki T, Sung M, Fukuda H, Kondo A (2006) Display of α-amylase on the surface of Lactobacillus casei cells by use of the PgsA anchor protein, and production of lactic acid from starch. Appl Environ Microbiol 72:269–275CrossRefGoogle Scholar
  29. 29.
    Okano K, Kimura S, Narita J, Fukuda H, Kondo A (2007) Improvement in lactic acid production from starch using α-amylase-secreting Lactococcus lactis cells adapted to maltose or starch. Appl Microbiol Biotechnol 75:1007–1013CrossRefGoogle Scholar
  30. 30.
    Kuipers OP, de Ruyter PG, Kleerebezem M, de Vos WM (1998) Quorum sensing-controlled gene expression in lactic acid bacteria. J Biotechnol 64:15–21CrossRefGoogle Scholar
  31. 31.
    Satoh E, Niimura Y, Uchimura T, Kozaki M, Komagata K (1993) Molecular cloning and expression of two alpha-amylase genes from Streptococcus bovis 148 in Escherichia coli. Appl Environ Microbiol 59:3669–3673Google Scholar
  32. 32.
    O’sullivan DJ, Klaenhammer TR (1993) Rapid mini-prep isolation of high-quality plasmid DNA from Lactococcus and Lactobacillus spp. Appl Environ Microbiol 59:2730–2733Google Scholar
  33. 33.
    Kleerebezem M, Beerthuyzen MM, Vaughan EE, de Vos WM, Kuipers OP (1997) Controlled gene expression systems for lactic acid bacteria: transferable nisin-inducible expression cassettes for Lactococcus, Leuconostoc, and Lactobacillus spp. Appl Environ Microbiol 63:4581–4584Google Scholar
  34. 34.
    DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  35. 35.
    Lapierre L, Germond JE, Ott A, Delley M, Mollet B (1999) D-Lactate dehydrogenase gene (ldhD) inactivation and resulting metabolic effects in the Lactobacillus johnsonii strains La1 and N312. Appl Environ Microbiol 65:4002–4007Google Scholar
  36. 36.
    Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano M, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85CrossRefGoogle Scholar
  37. 37.
    Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, Shakhova V, Grigoriev I, Lou Y, Rohksar D, Lucas S, Huang K, Goodstein DM, Hawkins T, Plengvidhya V, Welker D, Hughes J, Goh Y, Benson A, Baldwin K, Lee JH, Díaz-Muñiz I, Dosti B, Smeianov V, Wechter W, Barabote R, Lorca G, Altermann E, Barrangou R, Ganesan B, Xie Y, Rawsthorne H, Tamir D, Parker C, Breidt F, Broadbent J, Hutkins R, O’Sullivan D, Steele J, Unlu G, Saier M, Klaenhammer T, Richardson P, Kozyavkin S, Weimer B, Mills D (2006) Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci USA 103:15611–15616CrossRefGoogle Scholar
  38. 38.
    Wegmann U, O’Connell-Motherway M, Zomer A, Buist G, Shearman C, Canchaya C, Ventura M, Goesmann A, Gasson MJ, Kuipers OP, van Sinderen D, Kok J (2007) Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 189:3256–3270CrossRefGoogle Scholar
  39. 39.
    Gaspar P, Neves AR, Gasson MJ, Shearman CA, Santos H (2011) High yields of 2, 3-butanediol and mannitol in Lactococcus lactis through engineering of NAD + cofactor recycling. Appl Environ Microbiol 77:6826–6835CrossRefGoogle Scholar
  40. 40.
    Germond JE, Lapierre L, Delley M, Mollet B, Felis GE, Dellaglio F (2003) Evolution of the bacterial species Lactobacillus delbrueckii: a partial genomic study with reflections on prokaryotic species concept. Mol Biol Evol 20:93–104CrossRefGoogle Scholar
  41. 41.
    Lee DA, Collins EB (1976) Influence of temperature on growth of Streptococcus cremoris and Streptococcus lactis. J Dairy Sci 59:405–409CrossRefGoogle Scholar
  42. 42.
    Satoh E, Uchimura T, Kudo T, Komagata K (1997) Purification, characterization, and nucleotide sequence of an intracellular maltotriose-producing alpha-amylase from Streptococcus bovis 148. Appl Environ Microbiol 63:4941–4944Google Scholar
  43. 43.
    Kandasamy V, Vaidyanathan H, Djurdjevic I, Jayamani E, Ramachandran KB, Buckel W, Jayaraman G, Ramalingam S (2013) Engineering Escherichia coli with acrylate pathway genes for propionic acid synthesis and its impact on mixed-acid fermentation. Appl Microbiol Biotechnol 97:1191–1200CrossRefGoogle Scholar
  44. 44.
    Niu W, Kramer L, Mueller J, Liub K, Guo J (2019) Metabolic engineering of Escherichia coli for the de novo stereospecific biosynthesis of 1,2-propanediol through lactic acid. Metab Eng Commun 8:e00082CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biobased Materials ScienceKyoto Institute of TechnologyKyotoJapan

Personalised recommendations