Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Biologia




More options …
Volume 65, Issue 5

Issues

In-silico evidence of a pAO1 encoded pathway for the catabolism of tagatose derivatives in Arthrobacter nicotinovorans

Marius Mihăşan
  • Faculty of Biology, Department of Molecular and Experimental Biology, Alexandru Ioan Cuza University Iaşi, Bulevardul Carol I, Nr.11, 700506, Iasi, Romania
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2010-08-12 | DOI: https://doi.org/10.2478/s11756-010-0093-8

Abstract

Based on similarity searches, two putative pathways were previously described as being encoded by the pAO1 megaplasmid of Arthrobacter nicotinovorans: an almost fully established nicotine-degrading pathway and a yet unknown putative sugar-catabolic pathway. The general organization of the open reading frames (ORFs) of the latter indicated possible gene products as targets for docking experiments, aimed at identifying possible sugar substrates of this pathway. Homology modelling and docking results with the deduced proteins of three ORFs of the putative sugar catabolic pathway indicated D-tagatose-1,6-bisphosphate as a common ligand and thus as substrate of the pathway.

Keywords: homology modelling; in-silico docking; carbohydrates; Arthrobacter nicotinovorans

  • [1] Acher F.C. & Bertrand H. 2005. Amino acid recognition by Venus flytrap domains is encoded in an 8-residue motif. Biopolymers 80: 357–366. http://dx.doi.org/10.1002/bip.20229CrossrefGoogle Scholar

  • [2] Arnold K., Bordoli L., Kopp J. & Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195–201. http://dx.doi.org/10.1093/bioinformatics/bti770CrossrefGoogle Scholar

  • [3] Bates P.A., Kelley L.A., MacCallum R.M. & Sternberg M.J.E. 2001. Enhancement of protein modelling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins 45(Suppl. 5): 39–46. http://dx.doi.org/10.1002/prot.1168CrossrefGoogle Scholar

  • [4] Berman H., Henrick K. & Nakamura H. 2003. Announcing the worldwide Protein Data Bank. Nat. Struct. Biol. 10: 980. http://dx.doi.org/10.1038/nsb1203-980CrossrefGoogle Scholar

  • [5] Bröker D. & Steinbüchel A. 2009. Megaplasmid pKB1 of the rubber-degrading bacterium Gordonia westfalica strain Kb1. Microbial Megaplasmids 11: 297–309. http://dx.doi.org/10.1007/978-3-540-85467-8_14CrossrefGoogle Scholar

  • [6] Brühmüller M., Schimz A., Messmer L. & Decker K. 1975. Covalently bound FAD in D-6-hydroxynicotine oxidase. Immunological studies of D- and L-6-hydroxynicotine oxidase: evidence for a D-enzyme precursor. J. Biol. Chem. 250: 7747–77451. Google Scholar

  • [7] Cuneo M.J., Beese L.S. & Hellinga H.W. 2008. Ligand-induced conformational changes in a thermophilic ribose-binding protein. BMC Struct. Biol. 8: 50. http://dx.doi.org/10.1186/1472-6807-8-50CrossrefWeb of ScienceGoogle Scholar

  • [8] Dambe T.R., Kühn A.M., Brossette T., Giffhorn F. & Scheidig A.J. 2006. Crystal structure of NADP(H)-dependent 1,5-anhydro-D-fructose reductase from Sinorhizobium morelense at 2.2 Å resolution: construction of a NADH-accepting mutant and its application in rare sugar synthesis. Biochemistry 45: 10030–10042. http://dx.doi.org/10.1021/bi052589qCrossrefGoogle Scholar

  • [9] DiRusso C.C. & Nunn W.D. 1985. Cloning and characterization of a gene (fadR) involved in regulation of fatty acid metabolism in Escherichia coli. J. Bacteriol. 161: 583–588. Google Scholar

  • [10] Eaton A. 2001. Plasmid-encoded phthalate catabolic pathway in Arthrobacter keyseri 12B. J. Bacteriol. 183: 3689–3703. http://dx.doi.org/10.1128/JB.183.12.3689-3703.2001CrossrefGoogle Scholar

  • [11] Fukami-Kobayashi K., Tateno Y. & Nishikawa K. 2003. Parallel evolution of ligand specificity between LacI/GalR family repressors and periplasmic sugar-binding proteins. Mol. Biol. Evol. 20: 267–277. http://dx.doi.org/10.1093/molbev/msg038CrossrefGoogle Scholar

  • [12] Galkin A., Kulakova L., Melamud E., Li L., Wu C., Mariano P., Dunaway-Mariano D., Nash T. E. & Herzberg O. 2007. Characterization, kinetics, and crystal structures of fructose-1,6-bisphosphate aldolase from the human parasite, Giardia lamblia. J. Biol. Chem. 282: 4859–4867. http://dx.doi.org/10.1074/jbc.M609534200Web of ScienceCrossrefGoogle Scholar

  • [13] Gao Y., Suzuki H., Itou H., Zhou Y., Tanaka Y., Wachi M., Watanabe N., Tanaka I. & Yao M. 2008. Structural and functional characterization of the LldR from Corynebacterium glutamicum: a transcriptional repressor involved in L-lactate and sugar utilization. Nucleic Acids Res. 36: 7110–7123. http://dx.doi.org/10.1093/nar/gkn827Web of ScienceCrossrefGoogle Scholar

  • [14] Gorelik M., Lunin V.V., Skarina T. & Savchenko A. 2006. Structural characterization of GntR/HutC family signaling domain. Protein Sci. 15: 1506–1511. http://dx.doi.org/10.1110/ps.062146906CrossrefGoogle Scholar

  • [15] Guex N. & Peitsch M.C. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714–2723. http://dx.doi.org/10.1002/elps.1150181505CrossrefGoogle Scholar

  • [16] Haydon D.J. & Guest J.R. 1991 A new family of bacterial regulatory proteins, FEMS Microbiol. Lett. 63: 291–295. http://dx.doi.org/10.1111/j.1574-6968.1991.tb04544.xCrossrefGoogle Scholar

  • [17] Hillerich B. & Westpheling J. 2006. A new GntR family transcriptional regulator in Streptomyces coelicolor is required for morphogenesis and antibiotic production and controls transcription of an ABC transporter in response to carbon source. J. Bacteriol. 188: 7477–7487. http://dx.doi.org/10.1128/JB.00898-06CrossrefGoogle Scholar

  • [18] Holm L. & Park J. 2000. DaliLite workbench for protein structure comparison. Bioinformatics 16: 566–567. http://dx.doi.org/10.1093/bioinformatics/16.6.566CrossrefGoogle Scholar

  • [19] Igloi G. & Brandsch R. 2003. Sequence of the 165-kilobase catabolic plasmid pAO1 from Arthrobacter nicotinovorans and identification of a pAO1-dependent nicotine uptake system. J. Bacteriol. 185: 1976–1986. http://dx.doi.org/10.1128/JB.185.6.1976-1986.2003Google Scholar

  • [20] Jagusztyn-Krynicka E.K., Hansen J.B., Crow V.L., Thomas T.D., Honeyman A.L. & Curtiss 3rd R. 1992. Streptococcus mutans serotype c tagatose 6-phosphate pathway gene cluster. J. Bacteriol. 174: 6152–6158. Google Scholar

  • [21] Kendrew J.C., Bodo G., Dintzis H.M., Parrish R.G., Wyckoff H. & Phillips D.C. 1958. A three-dimensional model of the myoglobin molecule obtained by X-ray analysis. Nature 181: 662–666. http://dx.doi.org/10.1038/181662a0CrossrefGoogle Scholar

  • [22] Kentaro T. & Kanehisa M. 1998. A comparative analysis of ABC transporters in complete microbial genomes. Genome Res. 8: 1048–1059. Google Scholar

  • [23] Kingston R.L., Scopes R.K. & Baker E.N. 1996. The structure of glucose-fructose oxidoreductase from Zymomonas mobilis: an osmoprotective periplasmic enzyme containing nondissociable NADP. Structure 4: 1413–1428. http://dx.doi.org/10.1016/S0969-2126(96)00149-9CrossrefGoogle Scholar

  • [24] Kuntz I.D., Blaney J.M., Oatley S.J., Langridge R. & Ferrin T.E. 1982. A geometric approach to macromolecule-ligand interactions. J. Mol. Biol. 161: 269–288. http://dx.doi.org/10.1016/0022-2836(82)90153-XCrossrefGoogle Scholar

  • [25] Lang P.T., Brozell S.R., Mukherjee S., Pettersen E.F., Meng E.C., Thomas V., Rizzo R.C., Case D.A., James T.L. & Kuntz I.D. 2009. DOCK 6: combining techniques to model RNA-small molecule complexes. RNA 15: 1219–1230. http://dx.doi.org/10.1261/rna.1563609Web of ScienceCrossrefGoogle Scholar

  • [26] Laskowski R., MacArthur M., Moss D. & Thornton J. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26: 283–291. http://dx.doi.org/10.1107/S0021889892009944CrossrefGoogle Scholar

  • [27] Laurie A.T.R. & Jackson R.M. 2005. Q-SiteFinder: an energybased method for the prediction of protein-ligand binding sites. Bioinformatics 21: 1908–1916. http://dx.doi.org/10.1093/bioinformatics/bti315CrossrefGoogle Scholar

  • [28] Leite T.B., Gomes D., Miteva M.A., Chomilier J., Villoutreix B.O. & Tufféry P. 2007. Frog: a FRee Online druG 3D conformation generator. Nucleic Acids Res. 35(Web Server issue): W568–W572. http://dx.doi.org/10.1093/nar/gkm289CrossrefWeb of ScienceGoogle Scholar

  • [29] Mayer C. & Boos W. 2005. Hexose/pentose and hexitol/pentitol metabolism, EcoSal Module 3.4.1. In: Böck A., Curtiss 3rd R., Kaper J.B., Karp P.D., Neidhardt F.C., Nyström T., Slauch J.M., Squires C.L. & Ussery D. (eds), EcoSal — Escherichia coli and Salmonella: Cellular and Molecular Biology, Online Edition, ASM Press, Washington, DC. Google Scholar

  • [30] Miallau L., Hunter W.N., McSweeney S.M. & Leonard G.A. 2007. Structures of Staphylococcus aureus D-tagatose-6-phosphate kinase implicate domain motions in specificity and mechanism. J. Biol. Chem. 282: 19948–19957. http://dx.doi.org/10.1074/jbc.M701480200CrossrefWeb of ScienceGoogle Scholar

  • [31] Mihasan M., Artenie V. & Brandsch R. 2008. A monomeric aldehyde-dehydrogenase, part of the pAO1 encoded pathway for sugar utilization. FEBS J. 275(Issue s1): 285, Poster PP5E-4. Google Scholar

  • [32] Mihasan M., Artenie V. & Brandsch R. 2009. Characterization of a putative carbohydrate catabolic pathway of the megaplasmid pAO1 of Arthrobacter nicotinovorans. FEBS J. 276(Issue s1): 113, Poster P1-59. Google Scholar

  • [33] Oskouian B. & Stewart G.C. 1987. Cloning and characterization of the repressor gene of the Staphylococcus aureus lactose operon. J. Bacteriol. 169: 5459–5465. Google Scholar

  • [34] Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C. & Ferrin T.E. 2004. UCSF Chimera — a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605–1612. http://dx.doi.org/10.1002/jcc.20084CrossrefGoogle Scholar

  • [35] Rigali S., Derouaux A., Giannotta F. & Dusart J. 2002. Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J. Biol. Chem. 277: 12507–12515. http://dx.doi.org/10.1074/jbc.M110968200CrossrefGoogle Scholar

  • [36] Rigali S., Nothaft H., Noens E.E.E., Schlicht M., Colson S., Müller M., Joris B., Koerten H.K., Hopwood D.A., Titgemeyer F. & van Wezel G.P. 2006. The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol. Microbiol. 61: 1237–1251. http://dx.doi.org/10.1111/j.1365-2958.2006.05319.xCrossrefGoogle Scholar

  • [37] Rosey E.L., Oskouian B. & Stewart G.C. 1991. Lactose metabolism by Staphylococcus aureus: characterization of lacABCD, the structural genes of the tagatose 6-phosphate pathway. J. Bacteriol. 173: 5992–5998. Google Scholar

  • [38] Rosselló-Mora R.A., Lalucat J. & GarcÍa-Valdés E. 1994. Comparative biochemical and genetic analysis of naphthalene degradation among Pseudomonas stutzeri strains. Appl. Environ. Microbiol. 60: 966–972. Google Scholar

  • [39] van Aalten D.M., DiRusso C.C., Knudsen J. & Wierenga R.K. 2000. Crystal structure of FadR, a fatty acid-responsive transcription factor with a novel acyl coenzyme A-binding fold. EMBO J. 19: 5167–5177. http://dx.doi.org/10.1093/emboj/19.19.5167CrossrefGoogle Scholar

  • [40] Vedeler E. 2009. Megaplasmids and the degradation of aromatic compounds by soil bacteria. Microbial Megaplasmids 11: 33–53. http://dx.doi.org/10.1007/978-3-540-85467-8_2CrossrefGoogle Scholar

  • [41] Wiegert T., Sahm H. & Sprenger G.A. 1997. The substitution of a single amino acid residue (Ser-116◊Asp) alters NADPcontaining glucose-fructose oxidoreductase of Zymomonas mobilis into a glucose dehydrogenase with dual coenzyme specificity. J. Biol. Chem. 272: 13126–13133. http://dx.doi.org/10.1074/jbc.272.20.13126CrossrefGoogle Scholar

About the article

Published Online: 2010-08-12

Published in Print: 2010-10-01


Citation Information: Biologia, Volume 65, Issue 5, Pages 760–768, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.2478/s11756-010-0093-8.

Export Citation

© 2010 Slovak Academy of Sciences. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Comments (0)

Please log in or register to comment.
Log in