Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 13, pp 5079–5093 | Cite as

Glycerol metabolism and its regulation in lactic acid bacteria

  • Yuki DoiEmail author
Mini-Review

Abstract

Glycerol is one of the most important substrates involved in phospholipid biosynthesis, along with dihydroxyacetone phosphate (DHAP) as an intermediate of glycolysis. Organisms produce glycerol 3-phosphate (G3P) from endogenous DHAP and/or exogenous glycerol to synthesize glycerophospholipids from G3P. On the other hand, organisms can utilize glycerol as a carbon source to generate adenosine triphosphate (ATP). Glycerol metabolism in microorganisms has been investigated for > 50 years. The main research targets have been four bacteria that can utilize glycerol efficiently: Escherichia coli, Enterobacter aerogenes, Klebsiella pneumoniae, and Enterococcus faecalis. E. coli, E. aerogenes, and K. pneumoniae are gram-negative bacteria in the Enterobacteriales order of the class γ-Proteobacteria. In contrast, E. faecalis is a gram-positive bacterium in the Lactobacillales order of the class Bacilli, which are well-known lactic acid bacteria (LAB). Therefore, the glycerol metabolism of E. faecalis is characterized by the properties of both gram-positive bacteria and LAB, which substantially differ from the other three bacteria. As glycerophospholipids are essential for LAB, genes encoding the enzyme for glycerol metabolism (including G3P synthesis) are broadly detected from various LAB. However, these LAB’s classification and trend remained unclear until now, along with each LAB’s ability to utilize glycerol. Hence, the present review summarizes LAB’s glycerol metabolic pathway and regulation mechanism based on the distribution of the genes involved in those and discusses the peculiarities of glycerol metabolism in E. faecalis.

Keywords

Lactic acid bacteria Enterococcus faecalis Glycerol metabolism Metabolic regulation 

Notes

Compliance with ethical standards

Conflict of interest

The author declares that there is no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Alvarez M de F, Medina R, Pasteris SE, Strasser de Saad AM, Sesma F (2004) Glycerol metabolism of Lactobacillus rhamnosus ATCC 7469: cloning and expression of two glycerol kinase genes. J Mol Microbiol Biotechnol 7:170–181.  https://doi.org/10.1159/000079826 CrossRefGoogle Scholar
  2. Athenstaedt K, Daum G (1999) Phosphatidic acid, a key intermediate in lipid metabolism. Eur J Biochem 266:1–16.  https://doi.org/10.1046/j.1432-1327.1999.00822.x CrossRefGoogle Scholar
  3. Axelsson L (1998) Lactic acid bacteria: classification and physiology. In: Salminen S, Von Wright A (eds) Lactic acid bacteria: microbiology and functional aspects, 2nd edn. Marcel Dekker, New York, pp 1–72Google Scholar
  4. Bächler C, Schneider P, Bähler P, Lustig A, Erni B (2005) Escherichia coli dihydroxyacetone kinase controls gene expression by binding to transcription factor DhaR. EMBO J 24:283–293.  https://doi.org/10.1038/sj.emboj.7600517 CrossRefGoogle Scholar
  5. Bizzini A, Zhao C, Budin-Verneuil A, Sauvageot N, Giard JC, Auffray Y, Hartke A (2010) Glycerol is metabolized in a complex and strain-dependent manner in Enterococcus faecalis. J Bacteriol 192:779–785.  https://doi.org/10.1128/JB.00959-09 CrossRefGoogle Scholar
  6. Bouvet OM, Lenormand P, Ageron E, Grimont PA (1995) Taxonomic diversity of anaerobic glycerol dissimilation in the Enterobacteriaceae. Res Microbiol 146:279–290.  https://doi.org/10.1016/0923-2508(96)81051-5 CrossRefGoogle Scholar
  7. Claiborne A (1986) Studies on the structure and mechanism of Streptococcus faecium L-alpha-glycerophosphate oxidase. J Biol Chem 261:14398–14407Google Scholar
  8. Charrier V, Buckley E, Parsonage D, Galinier A, Darbon E, Jaquinod M, Forest E, Deutscher J, Claiborne A (1997) Cloning and sequencing of two enterococcal glpK genes and regulation of the encoded glycerol kinases by phosphoenolpyruvate-dependent, phosphotransferase system-catalyzed phosphorylation of a single histidyl residue. J Biol Chem 272:14166–14174.  https://doi.org/10.1074/jbc.272.22.14166 CrossRefGoogle Scholar
  9. Chen Z, Liu D (2016) Toward glycerol biorefinery: metabolic engineering for the production of biofuels and chemicals from glycerol. Biotechnol Biofuels 9:205.  https://doi.org/10.1186/s13068-016-0625-8 CrossRefGoogle Scholar
  10. Christen S, Srinivas A, Bähler P, Zeller A, Pridmore D, Bieniossek C, Baumann U, Erni B (2006) Regulation of the Dha operon of Lactococcus lactis: a deviation from the rule followed by the TetR family of transcription regulators. J Biol Chem 281:23129–23137.  https://doi.org/10.1074/jbc.M603486200 CrossRefGoogle Scholar
  11. Ciriminna R, Della Pina C, Rossi M, Pagliaro M (2014) Understanding the glycerol market. Eur J Lipid Sci Technol 116:1432–1439.  https://doi.org/10.1002/ejlt.201400229 CrossRefGoogle Scholar
  12. Cocaign-Bousquet M, Garrigues C, Loubiere P, Lindley ND (1996) Physiology of pyruvate metabolism in Lactococcus lactis. Antonie Van Leeuwenhoek 70:253–267.  https://doi.org/10.1007/BF00395936 CrossRefGoogle Scholar
  13. Coleman RA, Lee DP (2004) Enzymes of triacylglycerol synthesis and their regulation. Prog Lipid Res 43:134–176.  https://doi.org/10.1016/S0163-7827(03)00051-1 CrossRefGoogle Scholar
  14. Condon S (1987) Responses of lactic acid bacteria to oxygen. FEMS Microbiol Lett 46:269–280.  https://doi.org/10.1016/0378-1097(87)90112-1 CrossRefGoogle Scholar
  15. Daniel R, Boenigk R, Gottschalk G (1995a) Purification of 1,3-propanediol dehydrogenase from Citrobacter freundii and cloning, sequencing, and overexpression of the corresponding gene in Escherichia coli. J Bacteriol 177:2151–2156.  https://doi.org/10.1128/jb.177.8.2151-2156.1995 CrossRefGoogle Scholar
  16. Daniel R, Stuertz K, Gottschalk G (1995b) Biochemical and molecular characterization of the oxidative branch of glycerol utilization by Citrobacter freundii. J Bacteriol 177:4392–4401.  https://doi.org/10.1128/jb.177.15.4392-4401.1995 CrossRefGoogle Scholar
  17. Darbon E, Servant P, Poncet S, Deutscher J (2002) Antitermination by GlpP, catabolite repression via CcpA and inducer exclusion triggered by P-GlpK dephosphorylation control Bacillus subtilis glpFK expression. Mol Microbiol 43:1039–1052.  https://doi.org/10.1046/j.1365-2958.2002.02800.x CrossRefGoogle Scholar
  18. Deibel RH, Kvetkas MJ (1964) Fumarate reduction and its role in the diversion of glucose fermentation by Streptococcus faecalis. J Bacteriol 88:858–864Google Scholar
  19. Deutscher J, Bauer B, Sauerwald H (1993) Regulation of glycerol metabolism in Enterococcus faecalis by phosphoenolpyruvate-dependent phosphorylation of glycerol kinase catalyzed by enzyme I and HPr of the phosphotransferase system. J Bacteriol 175:3730–3733.  https://doi.org/10.1128/jb.175.12.3730-3733.1993 CrossRefGoogle Scholar
  20. Deutscher J, Sauerwald H (1986) Stimulation of dihydroxyacetone and glycerol kinase activity in Streptococcus faecalis by phosphoenolpyruvate-dependent phosphorylation catalyzed by enzyme I and HPr of the phosphotransferase system. J Bacteriol 166:829–836.  https://doi.org/10.1128/jb.166.3.829-836.1986 CrossRefGoogle Scholar
  21. Dobson R, Gray V, Rumbold K (2012) Microbial utilization of crude glycerol for the production of value-added products. J Ind Microbiol Biotechnol 39:217–226.  https://doi.org/10.1007/s10295-011-1038-0 CrossRefGoogle Scholar
  22. Doi Y (2015) L-lactate production from biodiesel-derived crude glycerol by metabolically engineered Enterococcus faecalis: cytotoxic evaluation of biodiesel waste and development of a glycerol-inducible gene expression system. Appl Environ Microbiol 81:2082–2089.  https://doi.org/10.1128/AEM.03418-14 CrossRefGoogle Scholar
  23. Doi Y (2018) Lactic acid fermentation is the main aerobic metabolic pathway in Enterococcus faecalis metabolizing a high concentration of glycerol. Appl Microbiol Biotechnol 102:10183–10192.  https://doi.org/10.1007/s00253-018-9351-4 CrossRefGoogle Scholar
  24. Doi Y, Ikegami Y (2014) Pyruvate formate-lyase is essential for fumarate-independent anaerobic glycerol utilization in the Enterococcus faecalis strain W11. J Bacteriol 196:2472–2480.  https://doi.org/10.1128/JB.01512-14 CrossRefGoogle Scholar
  25. Escapa IF, del Cerro C, García JL, Prieto MA (2013) The role of GlpR repressor in Pseudomonas putida KT2440 growth and PHA production from glycerol. Environ Microbiol 15:93–110.  https://doi.org/10.1111/j.1462-2920.2012.02790.x CrossRefGoogle Scholar
  26. Fernández M, Zúñiga M (2006) Amino acid catabolic pathways of lactic acid bacteria. Crit Rev Microbiol 32:155–183.  https://doi.org/10.1080/10408410600880643 CrossRefGoogle Scholar
  27. Fugelsang KC, Edwards CG (2007) Wine microbiology: practical applications and procedures. Springer, New YorkCrossRefGoogle Scholar
  28. Garcia-Alles LF, Siebold C, Nyffeler TL, Flükiger-Brühwiler K, Schneider P, Bürgi HB, Baumann U, Erni B (2004) Phosphoenolpyruvate- and ATP-dependent dihydroxyacetone kinases: covalent substrate-binding and kinetic mechanism. Biochemistry 43:13037–13045.  https://doi.org/10.1021/bi048575m CrossRefGoogle Scholar
  29. Garlapati VK, Shankar U, Budhiraja A (2015) Bioconversion technologies of crude glycerol to value added industrial products. Biotechnol Rep (Amst) 9:9–14.  https://doi.org/10.1016/j.btre.2015.11.002 CrossRefGoogle Scholar
  30. Garvie EI (1980) Bacterial lactate dehydrogenases. Microbiol Rev 44:106–139Google Scholar
  31. Gibellini F, Smith TK (2010) The Kennedy pathway−de novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life 62:414–428.  https://doi.org/10.1002/iub.337 CrossRefGoogle Scholar
  32. Green J, Paget MS (2004) Bacterial redox sensors. Nat Rev Microbiol 2:954–966.  https://doi.org/10.1038/nrmicro1022 CrossRefGoogle Scholar
  33. Gutknecht R, Beutler R, Garcia-Alles LF, Baumann U, Erni B (2001) The dihydroxyacetone kinase of Escherichia coli utilizes a phosphoprotein instead of ATP as phosphoryl donor. EMBO J 20:2480–2486.  https://doi.org/10.1093/emboj/20.10.2480 CrossRefGoogle Scholar
  34. Heller KB, Lin EC, Wilson TH (1980) Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol 144:274–278Google Scholar
  35. Houten SM, Wanders RJ (2010) A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation. J Inherit Metab Dis 33:469–477.  https://doi.org/10.1007/s10545-010-9061-2 CrossRefGoogle Scholar
  36. Hugenholtz J (1993) Citrate metabolism in lactic acid bacteria. FEMS Microbiol Rev 12:165–178.  https://doi.org/10.1016/0168-6445(93)90062-E CrossRefGoogle Scholar
  37. Iqbal J, Hussain MM (2009) Intestinal lipid absorption. Am J Physiol Endocrinol Metab 296:E1183–E1194.  https://doi.org/10.1152/ajpendo.90899.2008 CrossRefGoogle Scholar
  38. Javed S, Azeem F, Hussain S, Rasul I, Siddique MH, Riaz M, Afzal M, Kouser A, Nadeem H (2018) Bacterial lipases: a review on purification and characterization. Prog Biophys Mol Biol 132:23–34.  https://doi.org/10.1016/j.pbiomolbio.2017.07.014 CrossRefGoogle Scholar
  39. Jacobs NJ, VanDemark PJ (1960a) Comparison of the mechanism of glycerol oxidation in aerobically and anaerobically grown Streptococcus faecalis. J Bacteriol 79:532–538Google Scholar
  40. Jacobs NJ, VanDemark PJ (1960b) The purification and properties of the α-glycerophosphate-oxidizing enzyme of Streptococcus faecalis 10C1. Arch Biochem Biophys 88:250–255.  https://doi.org/10.1016/0003-9861(60)90230-7 CrossRefGoogle Scholar
  41. Jiang W, Wang S, Wang Y, Fang B (2016) Key enzymes catalyzing glycerol to 1,3-propanediol. Biotechnol Biofuels 9:57.  https://doi.org/10.1186/s13068-016-0473-6 CrossRefGoogle Scholar
  42. Johnson EA, Burke SK, Forage RG, Lin EC (1984) Purification and properties of dihydroxyacetone kinase from Klebsiella pneumoniae. J Bacteriol 160:55–60Google Scholar
  43. Johnson EA, Lin EC (1987) Klebsiella pneumoniae 1,3-propanediol: NAD+ oxidoreductase. J Bacteriol 169:2050–2554.  https://doi.org/10.1128/jb.169.5.2050-2054.1987 CrossRefGoogle Scholar
  44. Kajfasz JK, Mendoza JE, Gaca AO, Miller JH, Koselny KA, Giambiagi-Demarval M, Wellington M, Abranches J, Lemos JA (2012) The Spx regulator modulates stress responses and virulence in Enterococcus faecalis. Infect Immun 80:2265–2275.  https://doi.org/10.1128/IAI.00026-12 CrossRefGoogle Scholar
  45. Kandler O (1983) Carbohydrate metabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 49:209–224.  https://doi.org/10.1007/BF00399499 CrossRefGoogle Scholar
  46. Koditschek LK, Umbreit WW (1969) α-Glycerophosphate oxidase in Streptococcus faecium F 24. J Bacteriol 98:1063–1068Google Scholar
  47. Larson TJ, Cantwell JS, van Loo-Bhattacharya AT (1992) Interaction at a distance between multiple operators controls the adjacent, divergently transcribed glpTQ-glpACB operons of Escherichia coli K-12. J Biol Chem 267:6114–6121Google Scholar
  48. Leboeuf C, Leblanc L, Auffray Y, Hartke A (2000) Characterization of the ccpA gene of Enterococcus faecalis: identification of starvation-inducible proteins regulated by ccpA. J Bacteriol 182:5799–5806.  https://doi.org/10.1128/JB.182.20.5799-5806.2000 CrossRefGoogle Scholar
  49. Lin EC (1976) Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol 30:535–5378.  https://doi.org/10.1146/annurev.mi.30.100176.002535 CrossRefGoogle Scholar
  50. Liu WZ, Faber R, Feese M, Remington SJ, Pettigrew DW (1994) Escherichia coli glycerol kinase: role of a tetramer interface in regulation by fructose 1,6-bisphosphate and phosphotransferase system regulatory protein IIIglc. Biochemistry. 33:10120–10126.  https://doi.org/10.1021/bi00199a040 CrossRefGoogle Scholar
  51. Lindgren V, Rutberg L (1974) Glycerol metabolism in Bacillus subtilis: gene-enzyme relationships. J Bacteriol 119:431–442Google Scholar
  52. Ma F, Hanna MA (1999) Biodiesel production: a review. Bioresour Technol 70:1–15.  https://doi.org/10.1016/S0960-8524(99)00025-5 CrossRefGoogle Scholar
  53. Makarova KS, Koonin EV (2007) Evolutionary genomics of lactic acid bacteria. J Bacteriol 189:1199–1208.  https://doi.org/10.1128/JB.01351-06 CrossRefGoogle Scholar
  54. Marciniak BC, Pabijaniak M, de Jong A, Dűhring R, Seidel G, Hillen W, Kuipers OP (2012) High- and low-affinity cre boxes for CcpA binding in Bacillus subtilis revealed by genome-wide analysis. BMC Genomics 13:401.  https://doi.org/10.1186/1471-2164-13-401 CrossRefGoogle Scholar
  55. Murarka A, Dharmadi Y, Yazdani SS, Gonzalez R (2008) Fermentative utilization of glycerol by Escherichia coli and its implications for the production of fuels and chemicals. Appl Environ Microbiol 74:1124–1135.  https://doi.org/10.1128/AEM.02192-07 CrossRefGoogle Scholar
  56. Nicol RW, Marchand K, Lubitz WD (2012) Bioconversion of crude glycerol by fungi. Appl Microbiol Biotechnol 93:1865–1875.  https://doi.org/10.1007/s00253-012-3921-7 CrossRefGoogle Scholar
  57. Pagliaro M, Rossi M (2008) The future of glycerol. The Royal Society of Chemistry, RCS, UK.  https://doi.org/10.1039/9781847558305 Google Scholar
  58. Papadimitriou K, Alegría Á, Bron PA, de Angelis M, Gobbetti M, Kleerebezem M, Lemos JA, Linares DM, Ross P, Stanton C, Turroni F, van Sinderen D, Varmanen P, Ventura M, Zúñiga M, Tsakalidou E, Kok J (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80:837–890.  https://doi.org/10.1128/MMBR.00076-15 CrossRefGoogle Scholar
  59. Pfeiler EA, Klaenhammer TR (2007) The genomics of lactic acid bacteria. Trends Microbiol 15:546–553.  https://doi.org/10.1016/j.tim.2007.09.010 CrossRefGoogle Scholar
  60. Ranganathan SV, Narasimhan SL, Muthukumar K (2008) An overview of enzymatic production of biodiesel. Bioresour Technol 99:3975–3981.  https://doi.org/10.1016/j.biortech.2007.04.060 CrossRefGoogle Scholar
  61. Ravcheev DA, Li X, Latif H, Zengler K, Leyn SA, Korostelev YD, Kazakov AE, Novichkov PS, Osterman AL, Rodionov DA (2012) Transcriptional regulation of central carbon and energy metabolism in bacteria by redox-responsive repressor Rex. J Bacteriol 194:1145–1157.  https://doi.org/10.1128/JB.06412-11 CrossRefGoogle Scholar
  62. Riboulet-Bisson E, Hartke A, Auffray Y, Giard JC (2009) Ers controls glycerol metabolism in Enterococcus faecalis. Curr Microbiol 58:201–204.  https://doi.org/10.1007/s00284-008-9308-4 CrossRefGoogle Scholar
  63. Richey DP, Lin EC (1972) Importance of facilitated diffusion for effective utilization of glycerol by Escherichia coli. J Bacteriol 112:784–790Google Scholar
  64. Rivaldi JD, Sousa Silva M, Duarte LC, Ferreira AE, Cordeiro C, de Almeida Felipe MD, de Ponces Freire A, de Mancilha IM (2013) Metabolism of biodiesel-derived glycerol in probiotic Lactobacillus strains. Appl Microbiol Biotechnol 97:1735–1743.  https://doi.org/10.1007/s00253-012-4621-z CrossRefGoogle Scholar
  65. Ruch FE, Lengeler J, Lin EC (1974) Regulation of glycerol catabolism in Klebsiella aerogenes. J Bacteriol 119:50–56Google Scholar
  66. Ruch FE, Lin EC (1975) Independent constitutive expression of the aerobic and anaerobic pathways of glycerol catabolism in Klebsiella aerogenes. J Bacteriol 124:348–352Google Scholar
  67. Sakamoto M, Komagata K (1996) Aerobic growth of and activities of NADH oxidase and NADH peroxidase in lactic acid bacteria. J Ferment Bioeng 82:210–216.  https://doi.org/10.1111/j.1365-2672.2006.02955.x CrossRefGoogle Scholar
  68. Sauer M, Russmayer H, Grabherr R, Peterbauer CK, Marx H (2017) The efficient clade: lactic acid bacteria for industrial chemical production. Trends Biotechnol 35:756–769.  https://doi.org/10.1016/j.tibtech.2017.05.002 CrossRefGoogle Scholar
  69. Sauvageot N, Ladjouzi R, Benachour A, Rincé A, Deutscher J, Hartke A (2012) Aerobic glycerol dissimilation via the Enterococcus faecalis DhaK pathway depends on NADH oxidase and a phosphotransfer reaction from PEP to DhaK via EIIADha. Microbiology 158:2661–2666.  https://doi.org/10.1099/mic.0.061663-0 CrossRefGoogle Scholar
  70. Schryvers A, Lohmeier E, Weiner JH (1978) Chemical and functional properties of the native and reconstituted forms of the membrane-bound, aerobic glycerol-3-phosphate dehydrogenase of Escherichia coli. J Biol Chem 253(3):783–788Google Scholar
  71. Schweizer H, Boos W, Larson TJ (1985) Repressor for the sn-glycerol-3-phosphate regulon of Escherichia coli K-12: cloning of the glpR gene and identification of its product. J Bacteriol 161:563–566Google Scholar
  72. Schweizer HP, Po C (1996) Regulation of glycerol metabolism in Pseudomonas aeruginosa: characterization of the glpR repressor gene. J Bacteriol 178:5215–5221.  https://doi.org/10.1128/jb.178.17.5215-5221.1996 CrossRefGoogle Scholar
  73. Schweiger M, Schreiber R, Haemmerle G, Lass A, Fledelius C, Jacobsen P, Tornqvist H, Zechner R, Zimmermann R (2006) Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism. J Biol Chem 281:40236–40241.  https://doi.org/10.1074/jbc.M608048200
  74. Schütz H, Radler F (1984a) Anaerobic reduction of glycerol to propanediol-1.3 by Lactobacillus brevis and Lactobacillus buchneri. Syst Appl Microbiol 5:169–178.  https://doi.org/10.1016/S0723-2020(84)80018-1 CrossRefGoogle Scholar
  75. Schütz H, Radler F (1984b) Propanediol-1,2-dehydratase and metabolism of glycerol of Lactobacillus brevis. Arch Microbiol 139:366–370.  https://doi.org/10.1007/BF00408381 CrossRefGoogle Scholar
  76. Sriramulu DD, Liang M, Hernandez-Romero D, Raux-Deery E, Lünsdorf H, Parsons JB, Warren MJ, Prentice MB (2008) Lactobacillus reuteri DSM 20016 produces cobalamin-dependent diol dehydratase in metabolosomes and metabolizes 1,2-propanediol by disproportionation. J Bacteriol 190:4559–4567.  https://doi.org/10.1128/JB.01535-07 CrossRefGoogle Scholar
  77. Strittmatter CF (1959) Flavin-linked oxidative enzymes of Lactobacillus casei. J Biol Chem 234:2794–2800Google Scholar
  78. Subedi KP, Kim I, Kim J, Min B, Park C (2008) Role of GldA in dihydroxyacetone and methylglyoxal metabolism of Escherichia coli K12. FEMS Microbiol Lett 279:180–187.  https://doi.org/10.1111/j.1574-6968.2007.01032.x CrossRefGoogle Scholar
  79. Sweet G, Gandor C, Voegele R, Wittekindt N, Beuerle J, Truniger V, Lin EC, Boos W (1990) Glycerol facilitator of Escherichia coli: cloning of glpF and identification of the glpF product. J Bacteriol 172:424–430.  https://doi.org/10.1128/jb.172.1.424-430.1990 CrossRefGoogle Scholar
  80. Talarico TL, Axelsson LT, Novotny J, Fiuzat M, Dobrogosz WJ (1990) Utilization of glycerol as a hydrogen acceptor by Lactobacillus reuteri: purification of 1,3-propanediol: NAD oxidoreductase. Appl Environ Microbiol 56:943–948Google Scholar
  81. Talarico TL, Dobrogosz WJ (1990) Purification and characterization of glycerol dehydratase from Lactobacillus reuteri. Appl Environ Microbiol 56:1195–1197Google Scholar
  82. Toraya T, Kuno S, Fukui S (1980) Distribution of coenzyme B12-dependent diol dehydratase and glycerol dehydratase in selected genera of Enterobacteriaceae and Propionibacteriaceae. J Bacteriol 141:1439–1442Google Scholar
  83. Van Gerpen J (2005) Biodiesel processing and production. Fuel Process Technol 86:1097–1107.  https://doi.org/10.1016/j.fuproc.2004.11.005 CrossRefGoogle Scholar
  84. Varga ME, Weiner JH (1995) Physiological role of GlpB of anaerobic glycerol-3-phosphate dehydrogenase of Escherichia coli. Biochem Cell Biol 73:147–153.  https://doi.org/10.1139/o95-018 CrossRefGoogle Scholar
  85. Verneuil N, Rincé A, Sanguinetti M, Posteraro B, Fadda G, Auffray Y, Hartke A, Giard JC (2005a) Contribution of a PerR-like regulator to the oxidative-stress response and virulence of Enterococcus faecalis. Microbiology 151:3997–4004.  https://doi.org/10.1099/mic.0.28325-0 CrossRefGoogle Scholar
  86. Verneuil N, Rincé A, Sanguinetti M, Auffray Y, Hartke A, Giard JC (2005b) Implication of hypR in the virulence and oxidative stress response of Enterococcus faecalis. FEMS Microbiol Lett 252:137–141.  https://doi.org/10.1016/j.femsle.2005.08.043 CrossRefGoogle Scholar
  87. Vesić D, Kristich CJ (2013) A Rex family transcriptional repressor influences H2O2 accumulation by Enterococcus faecalis. J Bacteriol 195:1815–1824.  https://doi.org/10.1128/JB.02135-12 CrossRefGoogle Scholar
  88. Wang Q, Ingram LO, Shanmugam KT (2011) Evolution of D-lactate dehydrogenase activity from glycerol dehydrogenase and its utility for D-lactate production from lignocellulose. Proc Natl Acad Sci U S A 108:18920–18925.  https://doi.org/10.1073/pnas.1111085108 CrossRefGoogle Scholar
  89. Wang ZX, Zhuge J, Fang H, Prior BA (2001) Glycerol production by microbial fermentation: a review. Biotechnol Adv 19:201–223.  https://doi.org/10.1016/S0734-9750(01)00060-X CrossRefGoogle Scholar
  90. Warner JB, Lolkema JS (2003) CcpA-dependent carbon catabolite repression in bacteria. Microbiol Mol Biol Rev 67:475–490.  https://doi.org/10.1128/MMBR.67.4.475-490.2003 CrossRefGoogle Scholar
  91. Weissenborn DL, Wittekindt N, Larson TJ (1992) Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12. J Biol Chem 267(9):6122–6131Google Scholar
  92. Whittenbury R (1964) Hydrogen peroxide formation and catalase activity in the lactic acid bacteria. J Gen Microbiol 35:13–26.  https://doi.org/10.1099/00221287-35-1-13 CrossRefGoogle Scholar
  93. Yao J, Rock CO (2013) Phosphatidic acid synthesis in bacteria. Biochim Biophys Acta 1831:495–502.  https://doi.org/10.1016/j.bbalip.2012.08.018 CrossRefGoogle Scholar
  94. Yeh JI, Chinte U, Du S (2008) Structure of glycerol-3-phosphate dehydrogenase, an essential monotopic membrane enzyme involved in respiration and metabolism. Proc Natl Acad Sci U S A 105:3280–3285.  https://doi.org/10.1073/pnas.0712331105 CrossRefGoogle Scholar
  95. Zaunmüller T, Eichert M, Richter H, Unden G (2006) Variations in the energy metabolism of biotechnologically relevant heterofermentative lactic acid bacteria during growth on sugars and organic acids. Appl Microbiol Biotechnol 72:421–429.  https://doi.org/10.1007/s00253-006-0514-3 CrossRefGoogle Scholar
  96. Zielińska K, Fabiszewska A, Świątek M, Szymanowska-Powałowska D (2017) Evaluation of the ability to metabolize 1,2-propanediol by heterofermentative bacteria of the genus Lactobacillus. Electron J Biotechnol 26:60–63.  https://doi.org/10.1016/j.ejbt.2017.01.002 CrossRefGoogle Scholar
  97. Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6:222–233.  https://doi.org/10.1038/nrmicro1839 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Applied Chemistry and Biotechnology, Faculty of EngineeringOkayama University of ScienceOkayamaJapan

Personalised recommendations