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J Bacteriol. Oct 1993; 175(20): 6382–6391.
PMCID: PMC206745

Oxidation of D-lactate and L-lactate by Neisseria meningitidis: purification and cloning of meningococcal D-lactate dehydrogenase.

Abstract

Neisseria meningitidis was found to contain at least two lactate-oxidizing enzymes. One of these was purified 460-fold from spheroplast membranes and found to be specific primarily for D-lactate, with low-affinity activity for L-lactate. The gene for this enzyme (dld) was cloned, and a dld mutant was constructed by insertional inactivation of the gene. The mutant was unable to grow on D-lactate but retained the ability to grow on L-lactate, providing evidence for a second lactate-oxidizing enzyme with specificity for L-lactate. High-affinity L-lactate-oxidizing activity was detected in intact bacteria of both the dld+ and dld mutant strains. This L-lactate-oxidizing activity was also seen in sonicated bacteria but was reduced substantially on detergent solubilization or on preparation of spheroplast membranes.

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Selected References

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  • Allen PZ, Glode M, Schneerson R, Robbins JB. Identification of immunoglobulin heavy-chain isotypes of specific antibodies of horse 46 group B meningococcal antiserum. J Clin Microbiol. 1982 Feb;15(2):324–329. [PMC free article] [PubMed]
  • Allison N, O'Donnell MJ, Fewson CA. Membrane-bound lactate dehydrogenases and mandelate dehydrogenases of Acinetobacter calcoaceticus. Purification and properties. Biochem J. 1985 Oct 15;231(2):407–416. [PMC free article] [PubMed]
  • Bhatnagar RK, Hendry AT, Shanmugam KT, Jensen RA. The broad-specificity, membrane-bound lactate dehydrogenase of Neisseria gonorrhoeae: ties to aromatic metabolism. J Gen Microbiol. 1989 Feb;135(Pt 2):353–360. [PubMed]
  • Blake MS, Johnston KH, Russell-Jones GJ, Gotschlich EC. A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal Biochem. 1984 Jan;136(1):175–179. [PubMed]
  • Britigan BE, Klapper D, Svendsen T, Cohen MS. Phagocyte-derived lactate stimulates oxygen consumption by Neisseria gonorrhoeae. An unrecognized aspect of the oxygen metabolism of phagocytosis. J Clin Invest. 1988 Feb;81(2):318–324. [PMC free article] [PubMed]
  • Catlin BW. Genetic studies of sulfadiazine-resistant and methionine-requiring Neisseria isolated from clinical material. J Bacteriol. 1967 Sep;94(3):719–733. [PMC free article] [PubMed]
  • Catlin BW. Nutritional profiles of Neisseria gonorrhoeae, Neisseria meningitidis, and Neisseria lactamica in chemically defined media and the use of growth requirements for gonococcal typing. J Infect Dis. 1973 Aug;128(2):178–194. [PubMed]
  • CATLIN BW, SCHLOER GM. A defined agar medium for genetic transformation of Neisseria meningitidis. J Bacteriol. 1962 Mar;83:470–474. [PMC free article] [PubMed]
  • Chang AC, Cohen SN. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978 Jun;134(3):1141–1156. [PMC free article] [PubMed]
  • Davidson VL. Steady-state kinetic analysis of the quinoprotein methylamine dehydrogenase from Paracoccus denitrificans. Biochem J. 1989 Jul 1;261(1):107–111. [PMC free article] [PubMed]
  • Fernandez J, DeMott M, Atherton D, Mische SM. Internal protein sequence analysis: enzymatic digestion for less than 10 micrograms of protein bound to polyvinylidene difluoride or nitrocellulose membranes. Anal Biochem. 1992 Mar;201(2):255–264. [PubMed]
  • Frosch M, Schultz E, Glenn-Calvo E, Meyer TF. Generation of capsule-deficient Neisseria meningitidis strains by homologous recombination. Mol Microbiol. 1990 Jul;4(7):1215–1218. [PubMed]
  • Fu HS, Hassett DJ, Cohen MS. Oxidant stress in Neisseria gonorrhoeae: adaptation and effects on L-(+)-lactate dehydrogenase activity. Infect Immun. 1989 Jul;57(7):2173–2178. [PMC free article] [PubMed]
  • Futai M. Membrane D-lactate dehydrogenase from Escherichia coli. Purification and properties. Biochemistry. 1973 Jun 19;12(13):2468–2474. [PubMed]
  • Futai M, Kimura H. Inducible membrane-bound L-lactate dehydrogenase from Escherichia coli. Purification and properties. J Biol Chem. 1977 Aug 25;252(16):5820–5827. [PubMed]
  • Garvie EI. Bacterial lactate dehydrogenases. Microbiol Rev. 1980 Mar;44(1):106–139. [PMC free article] [PubMed]
  • Grossowicz N. Growth Requirements and Metabolism of Neisseria intracellularis. J Bacteriol. 1945 Jul;50(1):109–115. [PMC free article] [PubMed]
  • Hendry AT, Stewart IO. Auxanographic grouping and typing of Neisseria gonorrhoeae. Can J Microbiol. 1979 Apr;25(4):512–521. [PubMed]
  • Ho C, Pratt EA, Rule GS. Membrane-bound D-lactate dehydrogenase of Escherichia coli: a model for protein interactions in membranes. Biochim Biophys Acta. 1989 May 9;988(2):173–184. [PubMed]
  • Holten E, Jyssum K. Activities of some enzymes concerning pyruvate metabolism in Neisseria. Acta Pathol Microbiol Scand B Microbiol Immunol. 1974 Dec;82(6):843–848. [PubMed]
  • Hong JS, Kaback HR. Mutants of Salmonella typhimurium and Escherichia coli pleiotropically defective in active transport. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3336–3340. [PMC free article] [PubMed]
  • Hoshino E. L-serine enhances the anaerobic lactate metabolism of Veillonella dispar ATCC 17745. J Dent Res. 1987 Jun;66(6):1162–1165. [PubMed]
  • Hoshino E, Araya A. Lactate degradation by polysaccharide-producing Neisseria isolated from human dental plaque. Arch Oral Biol. 1980;25(3):211–212. [PubMed]
  • Hoshino E, Karino H, Yamada T. Lactate metabolism by human dental plaque and Veillonella under aerobic and anaerobic conditions. Arch Oral Biol. 1981;26(1):17–22. [PubMed]
  • Hoshino E, Yamada T, Araya S. Lactate degradation by a strain of Neisseria isolated from human dental plaque. Arch Oral Biol. 1976;21(11):677–683. [PubMed]
  • Ingledew WJ, Poole RK. The respiratory chains of Escherichia coli. Microbiol Rev. 1984 Sep;48(3):222–271. [PMC free article] [PubMed]
  • Johnston KH, Gotschlich EC. Isolation and characterization of the outer membrane of Neisseria gonorrhoeae. J Bacteriol. 1974 Jul;119(1):250–257. [PMC free article] [PubMed]
  • Juni E, Heym GA. Studies of some naturally occurring auxotrophs of Neisseria gonorrhoeae. J Gen Microbiol. 1980 Nov;121(1):85–92. [PubMed]
  • JYSSUM K. Intermediate reactions of the tricarboxylic acid cycle in meningococci. Acta Pathol Microbiol Scand. 1960;48:121–132. [PubMed]
  • Kohn LD, Kaback HR. Mechanisms of active transport in isolated bacterial membrane vesicles. XV. Purification and properties of the membrane-bound D-lactate dehydrogenase from Escherichia coli. J Biol Chem. 1973 Oct 25;248(20):7012–7017. [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. [PMC free article] [PubMed]
  • Long GL, Kaplan NO. D-lactate specific pyridine nucleotide lactate dehydrogenase in animals. Science. 1968 Nov 8;162(3854):685–686. [PubMed]
  • Lysko PG, Morse SA. Effects of steroid hormones on Neisseria gonorrhoeae. Antimicrob Agents Chemother. 1980 Aug;18(2):281–288. [PMC free article] [PubMed]
  • Markwell MA, Haas SM, Bieber LL, Tolbert NE. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem. 1978 Jun 15;87(1):206–210. [PubMed]
  • Massa EM, Leiva MA, Farías RN. Study of a time lag in the assay of Escherichia coli membrane-bound dehydrogenases based on tetrazolium salt reduction. Biochim Biophys Acta. 1985 Feb 4;827(2):150–156. [PubMed]
  • McGadey J. A tetrazolium method for non-specific alkaline phosphatase. Histochemie. 1970;23(2):180–184. [PubMed]
  • McLellan AC, Phillips SA, Thornalley PJ. Fluorimetric assay of D-lactate. Anal Biochem. 1992 Oct;206(1):12–16. [PubMed]
  • Morse SA, Cacciapuoti AF, Lysko PG. Physiology of Neisseria gonorrhoeae. Adv Microb Physiol. 1979;20:251–320. [PubMed]
  • Morse SA, Fitzgerald TJ. Effect of progesterone on Neisseria gonorrhoeae. Infect Immun. 1974 Dec;10(6):1370–1377. [PMC free article] [PubMed]
  • Murakami K, Gotschlich EC, Seiff ME. Cloning and characterization of the structural gene for the class 2 protein of Neisseria meningitidis. Infect Immun. 1989 Aug;57(8):2318–2323. [PMC free article] [PubMed]
  • Pratt EA, Fung LW, Flowers JA, Ho C. Membrane-bound D-lactate dehydrogenase from Escherichia coli: purification and properties. Biochemistry. 1979 Jan 23;18(2):312–316. [PubMed]
  • Rule GS, Pratt EA, Chin CC, Wold F, Ho C. Overproduction and nucleotide sequence of the respiratory D-lactate dehydrogenase of Escherichia coli. J Bacteriol. 1985 Mar;161(3):1059–1068. [PMC free article] [PubMed]
  • Santos E, Kung H, Young IG, Kaback HR. In vitro synthesis of the membrane-bound D-lactate dehydrogenase of Escherichia coli. Biochemistry. 1982 Apr 27;21(9):2085–2091. [PubMed]
  • Swanson J. Studies on gonococcus infection. XII. Colony color and opacity varienats of gonococci. Infect Immun. 1978 Jan;19(1):320–331. [PMC free article] [PubMed]
  • Tinsley CR, Manjula BN, Gotschlich EC. Purification and characterization of polyphosphate kinase from Neisseria meningitidis. Infect Immun. 1993 Sep;61(9):3703–3710. [PMC free article] [PubMed]
  • Vieira J, Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. [PubMed]
  • Wetzler LM, Gotschlich EC, Blake MS, Koomey JM. The construction and characterization of Neisseria gonorrhoeae lacking protein III in its outer membrane. J Exp Med. 1989 Jun 1;169(6):2199–2209. [PMC free article] [PubMed]
  • Winter DB, Morse SA. Physiology and metabolism of pathogenic Neisseria: partial characterization of the respiratory chain of Neisseria gonorrhoeae. J Bacteriol. 1975 Aug;123(2):631–636. [PMC free article] [PubMed]
  • Wong TP, Shockley RK, Johnston KH. WSJM, a simple chemically defined medium for growth of Neisseria gonorrhoeae. J Clin Microbiol. 1980 Apr;11(4):363–369. [PMC free article] [PubMed]
  • Young RA, Davis RW. Yeast RNA polymerase II genes: isolation with antibody probes. Science. 1983 Nov 18;222(4625):778–782. [PubMed]

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