Advertisement

Applied Microbiology and Biotechnology

, Volume 95, Issue 5, pp 1155–1163 | Cite as

Recent research on 3-phenyllactic acid, a broad-spectrum antimicrobial compound

  • Wanmeng MuEmail author
  • Shuhuai Yu
  • Lanjun Zhu
  • Tao Zhang
  • Bo Jiang
Mini-Review

Abstract

3-Phenyllactic acid (PLA), which is an organic acid widely existing in honey and lactic acid bacteria fermented food, can be produced by many microorganisms, especially lactic acid bacteria. It was proved as an ideal antimicrobial compound with broad and effective antimicrobial activity against both bacteria and fungi. In addition, it could be used as feed additives to replace antibiotics in livestock feeds. This article presented a review of recent studies on the existing resource, antimicrobial activity, and measurement of PLA. In addition, microorganism strains and dehydrogenases producing PLA were reviewed in detail, the metabolic pathway and regulation of PLA synthesis in LAB strains were discussed, and high-level bioproduction of PLA by microorganism fermentation was also summarized.

Keywords

3-Phenyllactic acid Antimicrobial compound Dehydrogenase Metabolic pathway Fermentation 

Notes

Acknowledgements

This work was supported by the 973 Project (No. 2012CB720802), the 863 Project (No. 2011AA100904), the Natural Science Foundation of China Project (No. 31171705), and the Support Project of Jiangsu Province (No. BE2011622, BE2011766, BE2010678, and BE2010626).

References

  1. Arai K, Kamata T, Uchikoba H, Fushinobu S, Matsuzawa H, Taguchi H (2001) Some Lactobacillus L-lactate dehydrogenases exhibit comparable catalytic activities for pyruvate and oxaloacetate. J Bacteriol 183:397–400CrossRefGoogle Scholar
  2. Armaforte E, Carri S, Ferri G, Caboni MF (2006) High-performance liquid chromatography determination of phenyllactic acid in MRS broth. J Chromatogr A 1131:281–284CrossRefGoogle Scholar
  3. Christidis Y, Schouteeten A (1985) Process for preparation of crystallized monohydrated sodium phenylpyruvate. US Patent 4,518,800Google Scholar
  4. Dallagnol AM, Catalan CAN, Mercado MI, de Valdez GF, Rollan GC (2011) Effect of biosynthetic intermediates and citrate on the phenyllactic and hydroxyphenyllactic acids production by Lactobacillus plantarum CRL 778. J Appl Microbiol 111:1447–1455CrossRefGoogle Scholar
  5. Dieuleveux V, Gueguen M (1998) Antimicrobial effects of D-3-phenyllactic acid on Listeria monocytogenes in TSB-YE medium, milk, and cheese. J Food Prot 61:1281–1285Google Scholar
  6. Dieuleveux V, Lemarinier S, Gueguen M (1998a) Antimicrobial spectrum and target site of D-3-phenyllactic acid. Int J Food Microbiol 40:177–183CrossRefGoogle Scholar
  7. Dieuleveux V, Van Der Pyl D, Chataud J, Gueguen M (1998b) Purification and characterization of anti-Listeria compounds produced by Geotrichum candidum. Appl Environ Microbiol 64:800–803Google Scholar
  8. Dimitrova B, Gevrenova R, Anklam E (2007) Analysis of phenolic acids in honeys of different floral origin by solid-phase extraction and high-performance liquid chromatography. Phytochem Anal 18:24–32CrossRefGoogle Scholar
  9. el Hawrani AS, Sessions RB, Moreton KM, Holbrook JJ (1996) Guided evolution of enzymes with new substrate specificities. J Mol Biol 264:97–110CrossRefGoogle Scholar
  10. Feil IK, Hendle J, Schomburg D (1997) Modified substrate specificity of L-hydroxyisocaproate dehydrogenase derived from structure-based protein engineering. Protein Eng 10:255–262CrossRefGoogle Scholar
  11. Garmyn D, Ferain T, Bernard N, Hols P, Delcour J (1995) Cloning, nucleotide sequence, and transcriptional analysis of the Pediococcus acidilactici L-(+)-lactate dehydrogenase gene. Appl Environ Microbiol 61:266–272Google Scholar
  12. Gerez CL, Carbajo MS, Rollan G, Torres Leal G, Font de Valdez G (2010) Inhibition of citrus fungal pathogens by using lactic acid bacteria. J Food Sci 75:354–359CrossRefGoogle Scholar
  13. Heil M, Podebrad F, Beck T, Mosandl A, Sewell AC, Bohles H (1998) Enantioselective multidimensional gas chromatography–mass spectrometry in the analysis of urinary organic acids. J Chromatogr B Biomed Sci Appl 714:119–126CrossRefGoogle Scholar
  14. Hummel W, Schutte H, Kula MR (1983) Large-scale production of D-lactate dehydrogenase for the stereospecific reduction of pyruvate and phenylpyruvate. Eur J Appl Microbiol Biotechnol 18:75–85CrossRefGoogle Scholar
  15. Hummel W, Schutte H, Kula MR (1985) D-2-hydroxyisocaproate dehydrogenase from Lactobacillus casei—a new enzyme suitable for stereospecific reduction of 2-ketocarboxylic acids. Appl Microbiol Biotechnol 21:7–15CrossRefGoogle Scholar
  16. Hummel W, Schutte H, Kula MR (1988) D-(−)-mandelic acid dehydrogenase from Labtobacillus curvatus. Appl Microbiol Biotechnol 28:433–439CrossRefGoogle Scholar
  17. Jia J, Mu W, Zhang T, Jiang B (2010) Bioconversion of phenylpyruvate to phenyllactate: gene cloning, expression, and enzymatic characterization of D- and L1-lactate dehydrogenases from Lactobacillus plantarum SK002. Appl Biochem Biotechnol 162:242–251CrossRefGoogle Scholar
  18. Kamata M, Toyomasu R, Suzuki D, Tanaka T (1986) D-phenyllactic acid production by Brevibacterium or Corynebacterium. Patent JP 86108396Google Scholar
  19. Kaneko KI, Hayashidani H, Ohtomo Y, Kosuge J, Kato M, Takahashi K, Shiraki Y, Ogawa M (1999) Bacterial contamination of ready-to-eat foods and fresh products in retail shops and food factories. J Food Prot 62:644–649Google Scholar
  20. Khan RI, Amin MR, Mohammed N, Onodera R (1998) Quantitative determination of aromatic amino acids and related compounds in rumen fluid by high-performance liquid chromatography. J Chromatogr B Biomed Sci Appl 710:17–25CrossRefGoogle Scholar
  21. Lavermicocca P, Valerio F, Evidente A, Lazzaroni S, Corsetti A, Gobbetti M (2000) Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl Environ Microbiol 66:4084–4090CrossRefGoogle Scholar
  22. Lavermicocca P, Valerio F, Visconti A (2003) Antifungal activity of phenyllactic acid against molds isolated from bakery products. Appl Environ Microbiol 69:634–640CrossRefGoogle Scholar
  23. Leng L, Zheng P, Sun Z (2006) Continuous production of l-phenylalanine from phenylpyruvic acid and l-aspartic acid by immobilized recombinant Escherichia coli SW0209-52. Process Biochem 41:1669–1672CrossRefGoogle Scholar
  24. 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 29:593–597CrossRefGoogle Scholar
  25. 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 56:2392–2399CrossRefGoogle Scholar
  26. Lind H, Sjogren J, Gohil S, Kenne L, Schnurer J, Broberg A (2007) Antifungal compounds from cultures of dairy propionibacteria type strains. FEMS Microbiol Lett 271:310–315CrossRefGoogle Scholar
  27. Matsunaga T, Higashijima M, Sulaswatty A, Nishimura S, Kitamura T, Tsuji M, Kawaguchi T (1987) Repeated batch production of L-phenylalanine from phenylpyruvate and NH4Cl by immobilized cells of Nocardia opaca under hydrogen high pressure. Biotechnol Bioeng 31:834–840CrossRefGoogle Scholar
  28. McSweeney PLH, Sousa MJ (2000) Biochemical pathways for the production of flavour compounds in cheeses during ripening: a review. Lait 80:293–324CrossRefGoogle Scholar
  29. Mu WM, Chen C, Li XF, Zhang T, Jiang B (2009a) Optimization of culture medium for the production of phenyllactic acid by Lactobacillus sp SK007. Bioresour Technol 100:1366–1370CrossRefGoogle Scholar
  30. Mu WM, Liu FL, Jia JH, Chen C, Zhang T, Jiang B (2009b) 3-Phenyllactic acid production by substrate feeding and pH-control in fed-batch fermentation of Lactobacillus sp SK007. Bioresour Technol 100:5226–5229CrossRefGoogle Scholar
  31. Mu W, Yu S, Jiang B, Li X (2012) Characterization of D-lactate dehydrogenase from Pediococcus acidilactici that converts phenylpyruvic acid into phenyllactic acid. Biotechnol Lett. doi: 10.1007/s10529-012-0847-1
  32. Nardi A, Eliseev A (1993) Use of charged and neutral cyclodextrins in capillary zone electrophoresis: enantiomeric resolution of some 2-hydroxy acids. J Chromatogr 638:247–253CrossRefGoogle Scholar
  33. Ndagano D, Lamoureux T, Dortu C, Vandermoten S, Thonart P (2011) Antifungal activity of 2 lactic acid bacteria of the Weissella genus isolated from food. J Food Sci 76:305–311CrossRefGoogle Scholar
  34. Ohhira I, Kuwaki S, Morita H, Suzuki T, Tomita S, Hisamatsu S, Sonoki S, Shinoda S (2004) Identification of 3-phenyllactic acid as a possible antibacterial substance produced by Enterococcus faecalis TH10. Biocontrol Sci 9:77–81CrossRefGoogle Scholar
  35. Prema P, Smila D, Palavesam A, Immanuel G (2010) Production and characterization of an antifungal compound (3-phenyllactic acid) produced by Lactobacillus plantarum strain. Food Bioprocess Tech 3:379–386CrossRefGoogle Scholar
  36. Rijnen L, Courtin P, Gripon JC, Yvon M (2000) Expression of a heterologous glutamate dehydrogenase gene in Lactococcus lactis highly improves the conversion of amino acids to aroma compounds. Appl Environ Microbiol 66:1354–1359CrossRefGoogle Scholar
  37. Riley RT, Norred WP, Bacon CW (1993) Fungal toxins in foods: recent concerns. Annu Rev Nutr 13:167–189CrossRefGoogle Scholar
  38. Rodriguez N, Salgado JM, Cortes S, Dominguez JM (2012) Antimicrobial activity of D-3-phenyllactic acid produced by fed-batch process against Salmonella enterica. Food Control 25:274–284CrossRefGoogle Scholar
  39. Ryan LA, Dal Bello F, Czerny M, Koehler P, Arendt EK (2009) Quantification of phenyllactic acid in wheat sourdough using high resolution gas chromatography–mass spectrometry. J Agric Food Chem 57:1060–1064CrossRefGoogle Scholar
  40. Sarkissian CN, Scriver CR, Mamer OA (2000) Measurement of phenyllactate, phenylacetate, and phenylpyruvate by negative ion chemical ionization–gas chromatography/mass spectrometry in brain of mouse genetic models of phenylketonuria and non-phenylketonuria hyperphenylalaninemia. Anal Biochem 280:242–249CrossRefGoogle Scholar
  41. Savijoki K, Palva A (1997) Molecular genetic characterization of the L-lactate dehydrogenase gene (ldhL) of Lactobacillus helveticus and biochemical characterization of the enzyme. Appl Environ Microbiol 63:2850–2856Google Scholar
  42. Schnürer J, Magnusson J (2005) Antifungal lactic acid bacteria as biopreservatives. Trends Food Sci Tech 16:70–78CrossRefGoogle Scholar
  43. Schnurer J, Olsson J, Borjesson T (1999) Fungal volatiles as indicators of food and feeds spoilage. Fungal Gen Biol 27:209–217CrossRefGoogle Scholar
  44. Schwenninger SM, Lacroix C, Truttmann S, Jans C, Sporndli C, Bigler L, Meile L (2008) Characterization of low-molecular-weight antiyeast metabolites produced by a food-protective Lactobacillus-Propionibacterium coculture. J Food Prot 71:2481–2487Google Scholar
  45. Strom K, Sjogren J, Broberg A, Schnurer J (2002) Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-4-OH-L-Pro) and 3-phenyllactic acid. Appl Environ Microbiol 68:4322–4327CrossRefGoogle Scholar
  46. Taguchi H, Ohta T (1991) D-lactate dehydrogenase is a member of the D-isomer-specific 2-hydroxyacid dehydrogenase family. Cloning, sequencing, and expression in Escherichia coli of the D-lactate dehydrogenase gene of Lactobacillus plantarum. J Biol Chem 266:12588–12594Google Scholar
  47. Tamura Y, Ohkubo A, Iwai S, Wada Y, Shinoda T, Arai K, Mineki S, Iida M, Taguchi H (2002) Two forms of NAD-dependent D-mandelate dehydrogenase in Enterococcus faecalis IAM 10071. Appl Environ Microbiol 68:947–951CrossRefGoogle Scholar
  48. Tan S, Wilkins A, Molan P, Holland P, Reid M (1988) A chemical approach to the determination of floral sources of New Zealand honeys. J Apicult Res 28:212–222Google Scholar
  49. Tekewe A, Singh S, Singh M, Mohan U, Banerjee UC (2008) Development and validation of HPLC method for the resolution of drug intermediates: DL-3-phenyllactic acid, DL-O-acetyl-3-phenyllactic acid and (+/−)-mexiletine acetamide enantiomers. Talanta 75:239–245CrossRefGoogle Scholar
  50. Tokuda C, Ishikura Y, Shigematsu M, Mutoh H, Tsuzuki S, Nakahira Y, Tamura Y, Shinoda T, Arai K, Takahashi O, Taguchi H (2003) Conversion of Lactobacillus pentosus D-lactate dehydrogenase to a D-hydroxyisocaproate dehydrogenase through a single amino acid replacement. J Bacteriol 185:5023–5026CrossRefGoogle Scholar
  51. Tuberoso CI, Bifulco E, Caboni P, Sarais G, Cottiglia F, Floris I (2011) Lumichrome and phenyllactic acid as chemical markers of thistle (Galactites tomentosa Moench) honey. J Agri Food Chem 59:364–369CrossRefGoogle Scholar
  52. Valerio F, Lavermicocca P, Pascale M, Visconti A (2004) Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol Lett 233:289–295CrossRefGoogle Scholar
  53. Van der Meulen R, Scheirlinck I, Van Schoor A, Huys G, Vancanneyt M, Vandamme P, De Vuyst L (2007) Population dynamics and metabolite target analysis of lactic acid bacteria during laboratory fermentations of wheat and spelt sourdoughs. Appl Environ Microbiol 73:4741–4750CrossRefGoogle Scholar
  54. 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 54:3832–3839CrossRefGoogle Scholar
  55. Wada Y, Iwai S, Tamura Y, Ando T, Shinoda T, Arai K, Taguchi H (2008) A new family of D-2-hydroxyacid dehydrogenases that comprises D-mandelate dehydrogenases and 2-ketopantoate reductases. Biosci Biotechnol Biochem 72:1087–1094CrossRefGoogle Scholar
  56. Wang J, Shao Y, Zhang Y, Jiao B, Dai H, Xue F (1991) Experimental studies of β-phenyllactic acid on the coronary system. J Shanghai Med Univ 18:295–297Google Scholar
  57. Wang JP, Yoo JS, Lee JH, Jang HD, Kim HJ, Shin SO, Seong SI, Kim IH (2009a) Effects of phenyllactic acid on growth performance, nutrient digestibility, microbial shedding, and blood profile in pigs. J Anim Sci 87:3235–3243CrossRefGoogle Scholar
  58. Wang JP, Yoo JS, Lee JH, Zhou TX, Jang HD, Kim HJ, Kim IH (2009b) Effects of phenyllactic acid on production performance, egg quality parameters, and blood characteristics in laying hens. J Appl Poultry Res 18:203–209CrossRefGoogle Scholar
  59. Wang JP, Lee JH, Yoo JS, Cho JH, Kim HJ, Kim IH (2010) Effects of phenyllactic acid on growth performance, intestinal microbiota, relative organ weight, blood characteristics, and meat quality of broiler chicks. Poultry Sci 89:1549–1555CrossRefGoogle Scholar
  60. Wang H, Yan Y, Wang J, Zhang H, Qi W (2012) Production and characterization of antifungal compounds produced by Lactobacillus plantarum IMAU10014. PloS one 7:e29452CrossRefGoogle Scholar
  61. Wilkins A, Lu Y, Tan S (1993) Extractives from New Zealand honeys. 4. Linalool derivatives and other components from nodding thistle (Carduus nutans) honey. J Agric Food Chem 41:873–878CrossRefGoogle Scholar
  62. Wilkins A, Lu Y, Tan S (1995) Extractives from New Zealand honeys. 5. Aliphatic dicarboxylic acids in New Zealand rewarewa (Knightea excelsa) honey. J Agric Food Chem 43:3021–3025CrossRefGoogle Scholar
  63. Yang G, Jing C, Zhu P, Hu X, Xu J, Wu Z, Yu X (2006) Molecular cloning and characterization of a novel lactate dehydrogenase gene from Clonorchis sinensis. Parasitol Res 99:55–64CrossRefGoogle Scholar
  64. Yu R, Van Scott E (1997) Method of using 3-phenyllactic acid for treating wrinkles. Patent US 5643953Google Scholar
  65. Yu S, Jiang H, Jiang B, Mu W (2012) Characterization of D-lactate dehydrogenase producing D-3-phenyllactic acid from Pediococcus pentosaceus. Biosci Biotechnol Biochem 76:853–855CrossRefGoogle Scholar
  66. Yvon M, Rijnen L (2001) Cheese flavour formation by amino acid catabolism. Int Dairy J 11:185–201CrossRefGoogle Scholar
  67. Yvon M, Thirouin S, Rijnen L, Fromentier D, Gripon JC (1997) An aminotransferase from Lactococcus lactis initiates conversion of amino acids to cheese flavor compounds. Appl Environ Microbiol 63:414–419Google Scholar
  68. Yvon M, Berthelot S, Gripon JC (1998) Adding alpha-ketoglutarate to semi-hard cheese curd highly enhances the conversion of amino acids to aroma compounds. Int Dairy J 8:889–898CrossRefGoogle Scholar
  69. Zhang DL, Li WL, Zhang JB, Tang WR, Chen XF, Cao KW, Chu QC, Ye JN (2010) Determination of unconjugated aromatic acids in urine by capillary electrophoresis with dual electrochemical detection—potential application in fast diagnosis of phenylketonuria. Electrophoresis 31:2989–2996CrossRefGoogle Scholar
  70. 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:e19030CrossRefGoogle Scholar
  71. Zhou Q, Shao WL (2010) Molecular genetic characterization of the thermostable L-lactate dehydrogenase gene (ldhL) of Thermoanaerobacter ethanolicus JW200 and biochemical characterization of the enzyme. Biochemistry (Mosc) 75:526–530CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Wanmeng Mu
    • 1
    Email author
  • Shuhuai Yu
    • 1
  • Lanjun Zhu
    • 1
  • Tao Zhang
    • 1
  • Bo Jiang
    • 1
  1. 1.State Key Laboratory of Food Science and TechnologyJiangnan UniversityWuxiChina

Personalised recommendations