Lactococcus lactis produces short-chain quinones that cross-feed Group B Streptococcus to activate respiration growth

Molecular Microbiology

Volumn 67, Issue 5, 2008, Pages 947-957

  Rezaïki, Lahcen ^a   Lamberet, Gilles ^a   Derré, Aurélie ^a   Gruss, Alexandra ^a   Gaudu, Philippe ^a  

^a CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; COPPER; ENZYME; HEME; IRON; MENAQUINONE; OXYGEN; QUINOL OXIDASE; QUINONE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; CCPA GENE; CELL METABOLISM; CONTROLLED STUDY; ECOSYSTEM; ELECTRON TRANSPORT; GENE; INTESTINE; LACTOCOCCUS LACTIS; MENB GENE; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; RESPIRATORY CHAIN; STREPTOCOCCUS GROUP C; VIRULENCE;

BACTERIAL PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COPPER; DNA-BINDING PROTEINS; ELECTRON TRANSPORT; GLYCOSIDE HYDROLASES; IRON; LACTOCOCCUS LACTIS; MUTATION; OXIDATIVE STRESS; OXYGEN; QUINONES; REPRESSOR PROTEINS; STREPTOCOCCUS AGALACTIAE; VITAMIN K 2;

BACTERIA (MICROORGANISMS); LACTOCOCCUS; LACTOCOCCUS LACTIS; STREPTOCOCCUS SP. 'GROUP B';

EID: 38849131354     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.06083.x     Document Type: Article

References (54)

1. Bader, M., Muse, W., Ballou, D.P., Gassner, C. Bardwell, J.C. (1999) Oxidative protein folding is driven by the electron transport system. Cell 98 : 217 227.
2. Bock, A. Gross, R. (2002) The unorthodox histidine kinases BvgS and EvgS are responsive to the oxidation status of a quinone electron carrier. Eur J Biochem 269 : 3479 3484.
3. Bolotin, A., Wincker, P., Mauger, S., Jaillon, O., Malarme, K., Weissenbach, J., et al. (2001) The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 11 : 731 753.
4. Collins, M.D. (1985) Analysis of isoprenoid quinones. Methods Microbiol 18 : 329 366.
5. Collins, M.D. Jones, D. (1979) The distribution of isoprenoid quinones in streptococci of serological groups D and N. J Gen Microbiol 114 : 27 33.
6. Collins, M.D. Jones, D. (1981) Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol Rev 45 : 316 354.
7. Coves, J. Fontecave, M. (1993) Reduction and mobilization of iron by a NAD(P)H:flavin oxidoreductase from Escherichia coli. Eur J Biochem 211 : 635 641.
8. Do, T.Q., Schultz, J.R. Clarke, C.F. (1996) Enhanced sensitivity of ubiquinone-deficient mutants of Saccharomyces cerevisiae to products of autoxidized polyunsaturated fatty acids. Proc Natl Acad Sci USA 93 : 7534 7539.
9. Duwat, P., Sourice, S., Cesselin, B., Lamberet, B., Vido, K., Gaudu, P., et al. (2001) Positive effects of heme and oxygen on growth and survival of the fermenting bacterium Lactococcus lactis. J Bacteriol 183 : 4509 4516.
10. Farrand, S.K. Taber, H.W. (1974) Changes in menaquinone concentration during growth and early sporulation in Bacillus subtilis. J Bacteriol 117 : 324 326.
11. Gasson, M. (1983) Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol 154 : 1 9.
12. Gaudu, P., Vido, K., Cesselin, B., Kulakauskas, S., Tremblay, J., Rezaiki, L., et al. (2002) Respiration capacity and consequences in Lactococcus lactis. Antonie Van Leeuwenhoek 82 : 263 269.
13. Gaudu, P., Lamberet, G., Poncet, S. Gruss, A. (2003) CcpA regulation of aerobic and respiration growth in Lactococcus lactis. Mol Microbiol 50 : 183 192.
14. Gennis, R.B. Stewart, V. (1996) Respiration. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt F. (ed.). Washington, DC : ASM Press, pp. 217 261.
15. Georgellis, D., Kwon, O. Lin, E.C. (2001) Quinones as the redox signal for the arc two-component system of bacteria. Science 292 : 2314 2316.
16. Glaser, P., Rusniok, C., Buchrieser, C., Chevalier, F., Frangeul, L., Msadek, T., et al. (2002) Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal disease. Mol Microbiol 45 : 1499 1513.
17. Graber, J.R. Breznak, J.A. (2005) Folate cross-feeding supports symbiotic homoacetogenic spirochetes. Appl Environ Microbiol 71 : 1883 1889.
18. Hess, A., Hollander, R. Mannheim, W. (1979) Lipoquinones of some spore-forming rods, lactic-acid bacteria and actinomycetes. J Gen Microbiol 115 : 247 252.
19. Holo, H. Nes, I. (1989) High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media. Appl Environ Microbiol 55 : 3119 3123.
20. Huycke, M.M., Moore, D., Joyce, W., Wise, P., Shepard, L., Kotake, Y. Gilmore, M.S. (2001) Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol 42 : 729 740.
21. Huycke, M.M., Abrams, V. Moore, D.R. (2002) Enterococcus faecalis produces extracellular superoxide and hydrogen peroxide that damages colonic epithelial cell DNA. Carcinogenesis 23 : 529 536.
22. Imlay, J.A. Fridovich, I. (1991) Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266 : 6957 6965.
23. Ivleva, N.B., Gao, T., LiWang, A.C. Golden, S.S. (2006) Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock. Proc Natl Acad Sci USA 103 : 17468 17473.
24. Jones, S.A., Chowdhury, F.Z., Fabich, A.J., Anderson, A., Schreiner, D.M., House, A.L., et al. (2007) Respiration of Escherichia coli in the mouse intestine. Infect Immun 75 : 4891 4899.
25. Kaneko, T., Takahashi, M. Suzuki, H. (1990) Acetoin fermentation by citrate-positive Lactococcus lactis subsp. lactis 3022 grown aerobically in the presence of hemin or Cu. Appl Environ Microbiol 56 : 2644 2649.
26. Kerr, T.J. Tritz, G.J. (1973) Cross-feeding of Escherichia coli mutants defective in the biosynthesis of nicotinamide adenine dinucleotide. J Bacteriol 115 : 982 986.
27. Klijn, N., Weerkamp, A.H. de Vos, W.M. (1995) Genetic marking of Lactococcus lactis shows its survival in the human gastrointestinal tract. Appl Environ Microbiol 61 : 2771 2774.
28. Korshunov, S. Imlay, J.A. (2006) Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J Bacteriol 188 : 6326 6334.
29. Kröger, A. Dadák, V. (1969) On the role of quinones in bacterial electron transport. The respiratory system of Bacillus megaterium. Eur J Biochem 11 : 328 340.
30. Lech, T. Sadlik, J.K. (2007) Copper concentration in body tissues and fluids in normal subjects of southern Poland. Biol Trace Elem Res 118 : 10 15.
31. Leloup, L., Ehrlich, S., Zagorec, M. Morel-Deville, F. (1997) Single-crossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsI and lacL genes. Appl Environ Microbiol 63 : 2117 2123.
32. Liang, P.H., Ko, T.P. Wang, A.H. (2002) Structure, mechanism and function of prenyltransferases. Eur J Biochem 269 : 3339 3354.
33. Ludwig, H., Rebhan, N., Blencke, H.M., Merzbacher, M. Stulke, J. (2002) Control of the glycolytic gapA operon by the catabolite control protein A in Bacillus subtilis: a novel mechanism of CcpA-mediated regulation. Mol Microbiol 45 : 543 553.
34. Luesink, E.J., van Herpen, R.E., Grossiord, B.P., Kuipers, O.P. de Vos, W.M. (1998) Transcriptional activation of the glycolytic las operon and catabolite repression of the gal operon in Lactococcus lactis are mediated by the catabolite control protein CcpA. Mol Microbiol 30 : 789 798.
35. Maruyama, A., Kumagai, Y., Morikawa, K., Taguchi, K., Hayashi, H. Ohta, T. (2003) Oxidative-stress-inducible qorA encodes an NADPH-dependent quinone oxidoreductase catalysing a one-electron reduction in Staphylococcus aureus. Microbiology 149 : 389 398.
36. Meganathan, R. (2001) Biosynthesis of menaquinone (vitamin K2) and ubiquinone (coenzyme Q): a perspective on enzymatic mechanisms. Vitam Horm 61 : 173 218.
37. Morishita, T., Tamura, N., Makino, T. Kudo, S. (1999) Production of menaquinones by lactic acid bacteria. J Dairy Sci 82 : 1897 1903.
38. Myers, C.R. Myers, J.M. (2004) Shewanella oneidensis MR-1 restores menaquinone synthesis to a menaquinone-negative mutant. Appl Environ Microbiol 70 : 5415 5425.
39. Newman, D.K. Kolter, R. (2000) A role for excreted quinones in extracellular electron transfer. Nature 405 : 94 97.
40. Okada, K., Kainou, T., Matsuda, H. Kawamukai, M. (1998) Biological significance of the side chain length of ubiquinone in Saccharomyces cerevisiae. FEBS Lett 431 : 241 244.
41. Qin, X. Taber, H.W. (1996) Transcriptional regulation of the Bacillus subtilis menp1 promoter. J Bacteriol 178 : 705 713.
42. Rapisarda, V.A., Montelongo, L.R., Farias, R.N. Massa, E.M. (1999) Characterization of an NADH-linked cupric reductase activity from the Escherichia coli respiratory chain. Arch Biochem Biophys 370 : 143 150.
43. Rezaiki, L., Cesselin, B., Yamamoto, Y., Vido, K., van West, E., Gaudu, P. Gruss, A. (2004) Respiration metabolism reduces oxidative and acid stress to improve long-term survival of Lactococcus lactis. Mol Microbiol 53 : 1331 1342.
44. Rouault, T.A. (2004) Microbiology. Pathogenic bacteria prefer heme. Science 305 : 1577 1578.
45. Saffarini, D.A., Blumerman, S.L. Mansoorabadi, K.J. (2002) Role of menaquinones in Fe(III) reduction by membrane fractions of Shewanella putrefaciens. J Bacteriol 184 : 846 848.
46. Sato, T., Yamada, Y., Ohtani, Y., Mitsui, N., Murasawa, H. Araki, S. (2001) Production of menaquinone (vitamin K2)-7 by Bacillus subtilis. J Biosci Bioeng 91 : 16 20.
47. Simon, D. Chopin, A. (1988) Construction of a vector plasmid family and its use for molecular cloning in Streptococcus lactis. Biochimie 70 : 559 566.
48. Soballe, B. Poole, R.K. (2000) Ubiquinone limits oxidative stress in Escherichia coli. Microbiology 146 : 787 796.
49. Spellerberg, B. (2000) Pathogenesis of neonatal Streptococcus agalactiae infections. Microbes Infect 2 : 1733 1742.
50. Taber, H. (1993) Bacillus subtilis and other gram-positive bacteria. In Biochemistry and Molecular Genetics. Sonenshein A.L., Joch J.A. Losick R. (eds). Washington, DC : ASM Press, pp. 199 212.
51. Wang, G. Maier, R.J. (2004) An NADPH quinone reductase of Helicobacter pylori plays an important role in oxidative stress resistance and host colonization. Infect Immun 72 : 1391 1396.
52. Wegmann, U., O'Connell-Motherway, M., Zomer, A., Buist, G., Shearman, C., Canchaya, C., et al. (2007) Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 189 : 3256 3270.
53. Yamamoto, Y., Poyart, C., Trieu-Cuot, P., Lamberet, G., Gruss, A. Gaudu, P. (2005) Respiration metabolism of Group B Streptococcus is activated by environmental haem and quinone and contributes to virulence. Mol Microbiol 56 : 525 534.
54. Zomer, A.L., Buist, G., Larsen, R., Kok, J. Kuipers, O.P. (2007) Time-resolved determination of the CcpA regulon of Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 189 : 1366 1381.