User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Lactate racemase is a nickel-dependent enzyme activated by a widespread maturation system.

Primary tabs

Desguin, Benoît [UCL] Goffin, Philippe Viaene, Eric Kleerebezem, Michiel Martin-Diaconescu, Vlad Soumillion, Patrice [UCL] Hols, Pascal [UCL]

Racemases catalyse the inversion of stereochemistry in biological molecules, giving the organism the ability to use both isomers. Among them, lactate racemase remains unexplored due to its intrinsic instability and lack of molecular characterization. Here we determine the genetic basis of lactate racemization in Lactobacillus plantarum. We show that, unexpectedly, the racemase is a nickel-dependent enzyme with a novel α/β fold. In addition, we decipher the process leading to an active enzyme, which involves the activation of the apo-enzyme by a single nickel-containing maturation protein that requires preactivation by two other accessory proteins. Genomic investigations reveal the wide distribution of the lactate racemase system among prokaryotes, showing the high significance of both lactate enantiomers in carbon metabolism. The even broader distribution of the nickel-based maturation system suggests a function beyond activation of the lactate racemase and possibly linked with other undiscovered nickel-dependent enzymes.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2014
Language Anglais
Journal information "Nature Communications" - Vol. 5, p. 3615 (2014)
Peer reviewed yes
Publisher Nature Publishing Group (London)
e-issn 2041-1723
Publication status Publié
Affiliations UCL - SST/ISV - Institut des sciences de la vie
UCL - SST/LIBST - Louvain Institute of Biomolecular Science and Technology
Links
  1. Okano Kenji, Tanaka Tsutomu, Ogino Chiaki, Fukuda Hideki, Kondo Akihiko, Biotechnological production of enantiomeric pure lactic acid from renewable resources: recent achievements, perspectives, and limits, 10.1007/s00253-009-2280-5
  2. Thauer R. K., Bacteriol. Rev., 41, 100 (1977)
  3. Walsh C., Vancomycin resistance: decoding the molecular logic, 10.1126/science.8392747
  4. Goffin P., Deghorain M., Mainardi J.-L., Tytgat I., Champomier-Verges M.-C., Kleerebezem M., Hols P., Lactate Racemization as a Rescue Pathway for Supplying D-Lactate to the Cell Wall Biosynthesis Machinery in Lactobacillus plantarum, 10.1128/jb.187.19.6750-6761.2005
  5. Garvie E. I., Microbiol. Rev., 44, 106 (1980)
  6. Tatum Edward Lawrie, Peterson William Harold, Fred Edwin Broun, Enzymic racemization of optically active lactic acid, 10.1042/bj0301892
  7. Stetter K. O., Kandler O., Untersuchungen zur Entstehung von Dl-Milchs�ure bei Lactobacillen und Charakterisierung einer Milchs�ureracemase bei einigen Arten der Untergattung Streptobacterium, 10.1007/bf00417453
  8. Oren Aharon, Gurevich Peter, Diversity of lactate metabolism in halophilic archaea, 10.1139/m95-042
  9. Hino T., Appl. Environ. Microbiol., 59, 255 (1993)
  10. Gilmour M., Flint H. J., Mitchell W. J., Multiple lactate dehydrogenase activities of the rumen bacterium Selenomonas ruminantium, 10.1099/13500872-140-8-2077
  11. Nagar Mitesh, Narmandakh Ariun, Khalak Yuriy, Bearne Stephen L., Redefining the Minimal Substrate Tolerance of Mandelate Racemase. Racemization of Trifluorolactate, 10.1021/bi201188j
  12. Cava Felipe, Lam Hubert, de Pedro Miguel A., Waldor Matthew K., Emerging knowledge of regulatory roles of d-amino acids in bacteria, 10.1007/s00018-010-0571-8
  13. Richard John P., Amyes Tina L., On the importance of being zwitterionic: enzymatic catalysis of decarboxylation and deprotonation of cationic carbon, 10.1016/j.bioorg.2004.05.002
  14. Hiyama T., J. Biochem., 64, 99 (1968)
  15. KATAGIRI Hideo, SUGIMORI Tsunetake, IMAI Kazutami, On the Metabolism of Organic Acids by Clostridium acetobutylicum, 10.1271/bbb1961.25.281
  16. Dennis D., Biochem. Z., 338, 485 (1963)
  17. Cantwell Allan, Dennis Don, Lactate racemase. Direct evidence for an α-carbonyl intermediate, 10.1021/bi00699a009
  18. Bienert Gerd P., Desguin Benoît, Chaumont François, Hols Pascal, Channel-mediated lactic acid transport: a novel function for aquaglyceroporins in bacteria, 10.1042/bj20130388
  19. Rodionov D. A., Hebbeln P., Gelfand M. S., Eitinger T., Comparative and Functional Genomic Analysis of Prokaryotic Nickel and Cobalt Uptake Transporters: Evidence for a Novel Group of ATP-Binding Cassette Transporters, 10.1128/jb.188.1.317-327.2006
  20. Boer Jodi L., Mulrooney Scott B., Hausinger Robert P., Nickel-dependent metalloenzymes, 10.1016/j.abb.2013.09.002
  21. Giedroc David P., Cornish Peter V., Frameshifting RNA pseudoknots: Structure and mechanism, 10.1016/j.virusres.2008.06.008
  22. McCall Keith A., Fierke Carol A., Colorimetric and Fluorimetric Assays to Quantitate Micromolar Concentrations of Transition Metals, 10.1006/abio.2000.4706
  23. Tseng C. P., J. Bacteriol., 173, 4411 (1991)
  24. Li Yanjie, Zamble Deborah B., Nickel Homeostasis and Nickel Regulation: An Overview, 10.1021/cr900010n
  25. Andreeva A., Howorth D., Chandonia J.-M., Brenner S. E., Hubbard T. J. P., Chothia C., Murzin A. G., Data growth and its impact on the SCOP database: new developments, 10.1093/nar/gkm993
  26. Colpas Gerard J., Maroney Michael J., Bagyinka Csaba., Kumar Manoj., Willis William S., Suib Steven L., Mascharak Pradip K., Baidya Narayan., X-ray spectroscopic studies of nickel complexes, with application to the structure of nickel sites in hydrogenases, 10.1021/ic00005a010
  27. Teusink Bas, Wiersma Anne, Molenaar Douwe, Francke Christof, de Vos Willem M., Siezen Roland J., Smid Eddy J., Analysis of Growth ofLactobacillus plantarumWCFS1 on a Complex Medium Using a Genome-scale Metabolic Model, 10.1074/jbc.m606263200
  28. The Prokaryotes, Ch. 13, 354 (2006)
  29. The Prokaryotes, Ch. 22, 659 (2007)
  30. Call D. F., Logan B. E., Lactate Oxidation Coupled to Iron or Electrode Reduction by Geobacter sulfurreducens PCA, 10.1128/aem.06434-11
  31. Duncan S. H., Louis P., Flint H. J., Lactate-Utilizing Bacteria, Isolated from Human Feces, That Produce Butyrate as a Major Fermentation Product, 10.1128/aem.70.10.5810-5817.2004
  32. Zhang Yan, Rodionov Dmitry A, Gelfand Mikhail S, Gladyshev Vadim N, Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization, 10.1186/1471-2164-10-78
  33. Gibrat Jean-Francois, Madej Thomas, Bryant Stephen H, Surprising similarities in structure comparison, 10.1016/s0959-440x(96)80058-3
  34. Lim L. W., J. Biol. Chem., 261, 15140 (1986)
  35. Kozbial Piotr Z, Mushegian Arcady R, 10.1186/1472-6807-5-19
  36. Kuchenreuther Jon M., Britt R. David, Swartz James R., New Insights into [FeFe] Hydrogenase Activation and Maturase Function, 10.1371/journal.pone.0045850
  37. Barton Bryan E., Rauchfuss Thomas B., Hydride-Containing Models for the Active Site of the Nickel−Iron Hydrogenases, 10.1021/ja105312p
  38. Dower W. J., Miller J. F., Ragsdale C. W., High efficiency transformation of E.coli by high voltage electroporation, 10.1093/nar/16.13.6127
  39. Lambert J. M., Bongers R. S., Kleerebezem M., Cre-lox-Based System for Multiple Gene Deletions and Selectable-Marker Removal in Lactobacillus plantarum, 10.1128/aem.01473-06
  40. Holo H., Appl. Environ. Microbiol., 55, 3119 (1989)
  41. Trower M., Methods in Molecular Biology, Vol. 31, 19 (1994)
  42. Ferain T., J. Bacteriol., 178, 5431 (1996)
  43. Stevens M. J. A., Wiersma A., de Vos W. M., Kuipers O. P., Smid E. J., Molenaar D., Kleerebezem M., Improvement of Lactobacillus plantarum Aerobic Growth as Directed by Comprehensive Transcriptome Analysis, 10.1128/aem.00136-08
  44. Bradford Marion M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, 10.1016/0003-2697(76)90527-3
  45. Jones L. J., Biotechniques, 34, 850 (2003)
  46. Shapiro Arnold L., Viñuela Eladio, V. Maizel Jacob, Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels, 10.1016/0006-291x(67)90391-9
  47. Duby Geoffrey, Degand Hervé, Faber Anne-Marie, Boutry Marc, The proteome complement of Nicotiana tabacum Bright-Yellow-2 culture cells, 10.1002/pmic.200900527
  48. Schmidt Thomas GM, Skerra Arne, The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins, 10.1038/nprot.2007.209
  49. Mueller-Dieckmann Jochen, The open-access high-throughput crystallization facility at EMBL Hamburg, 10.1107/s0907444906038121
  50. Kabsch W., Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants, 10.1107/s0021889893005588
  51. Panjikar Santosh, Parthasarathy Venkataraman, Lamzin Victor S., Weiss Manfred S., Tucker Paul A., Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment, 10.1107/s0907444905001307
  52. Schneider Thomas R., Sheldrick George M., Substructure solution withSHELXD, 10.1107/s0907444902011678
  53. Sheldrick G. M., Macromolecular phasing with SHELXE, 10.1524/zkri.217.12.644.20662
  54. McCoy Airlie J., Grosse-Kunstleve Ralf W., Adams Paul D., Winn Martyn D., Storoni Laurent C., Read Randy J., Phasercrystallographic software, 10.1107/s0021889807021206
  55. Murshudov G. N., Vagin A. A., Dodson E. J., Refinement of Macromolecular Structures by the Maximum-Likelihood Method, 10.1107/s0907444996012255
  56. Collaborative Computational Project, Number 4, The CCP4 suite: programs for protein crystallography, 10.1107/s0907444994003112
  57. Terwilliger Thomas, SOLVE and RESOLVE: automated structure solution, density modification and model building, 10.1107/s0909049503023938
  58. Morris Richard J., Perrakis Anastassis, Lamzin Victor S., ARP⧸wARP and Automatic Interpretation of Protein Electron Density Maps, Methods in Enzymology (2003) ISBN:9780121827779 p.229-244, 10.1016/s0076-6879(03)74011-7
  59. Emsley Paul, Cowtan Kevin, Coot: model-building tools for molecular graphics, 10.1107/s0907444904019158
  60. Webb S. M., SIXPack a Graphical User Interface for XAS Analysis Using IFEFFIT, 10.1238/physica.topical.115a01011
  61. Ravel B., Newville M., ATHENA,ARTEMIS,HEPHAESTUS: data analysis for X-ray absorption spectroscopy usingIFEFFIT, 10.1107/s0909049505012719
  62. Newville Matthew, EXAFS analysis usingFEFFandFEFFIT, 10.1107/s0909049500016290
  63. Zabinsky S. I., Rehr J. J., Ankudinov A., Albers R. C., Eller M. J., Multiple-scattering calculations of x-ray-absorption spectra, 10.1103/physrevb.52.2995
  64. Engh R. A., Huber R., Accurate bond and angle parameters for X-ray protein structure refinement, 10.1107/s0108767391001071
  65. Blackburn N. J., J. Biol. Chem., 266, 23120 (1991)
  66. Ferreira Gloria C., Franco Ricardo, Mangravita Arianna, George Graham N., Unraveling the Substrate−Metal Binding Site of Ferrochelatase:  An X-ray Absorption Spectroscopic Study†, 10.1021/bi015814m
  67. Martin-Diaconescu Vlad, Bellucci Matteo, Musiani Francesco, Ciurli Stefano, Maroney Michael J., Unraveling the Helicobacter pylori UreG zinc binding site using X-ray absorption spectroscopy (XAS) and structural modeling, 10.1007/s00775-011-0857-9
  68. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G., Clustal W and Clustal X version 2.0, 10.1093/bioinformatics/btm404
  69. Saitou N., Mol. Biol. Evol., 4, 406 (1987)
Bibliographic reference Desguin, Benoît ; Goffin, Philippe ; Viaene, Eric ; Kleerebezem, Michiel ; Martin-Diaconescu, Vlad ; et. al. Lactate racemase is a nickel-dependent enzyme activated by a widespread maturation system.. In: Nature Communications, Vol. 5, p. 3615 (2014)
Permanent URL http://hdl.handle.net/2078.1/156031