A novel Dps-type protein from insect gut bacteria catalyses hydrolysis and synthesis of N-acyl amino acids

Environmental Microbiology

Volumn 9, Issue 6, 2007, Pages 1572-1583

  Ping, Liyan ^a   Büchler, Rita ^a   Mithöfer, Axel ^a   Svatoš, Aleš ^a   Spiteller, Dieter ^a   Dettner, Konrad ^b   Gmeiner, Sophie ^b   Piel, Jörn ^c   Schlott, Bernhard ^d   Boland, Wilhelm ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b UNIVERSITY OF BAYREUTH   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; AMINO ACID; BACTERIAL PROTEIN; DNA BINDING PROTEIN; DPS PROTEIN, BACTERIA; UNCLASSIFIED DRUG;

ABDOMEN; ACTINOMYCETALES; ANIMAL; ARTICLE; CATALYSIS; CHEMISTRY; ENZYMOLOGY; GENETICS; HYDROLYSIS; INSECT; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY;

ABDOMEN; ACTINOMYCETALES; AMIDOHYDROLASES; AMINO ACIDS; ANIMALS; BACTERIAL PROTEINS; CATALYSIS; DNA-BINDING PROTEINS; HYDROLYSIS; INSECTS;

HEXAPODA; MICROBACTERIUM ARBORESCENS; SPODOPTERA EXIGUA;

EID: 34248587974     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2007.01279.x     Document Type: Article

References (54)

1. Alborn, T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276 : 945 949.
2. Alborn, H.T., Jones, T.H., Stenhagen, G.S. Tumlinson, J.H. (2000) Identification and synthesis of volicitin and related components from beet armyworm oral secretions. J Chem Ecol 26 : 203 220.
3. Almirón, M., Link, A.J., Furlong, D. Kolter, R. (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6 : 2646 2654.
4. Billen, D. Hewitt, R. (1966) Influence of starvation for methionine and other amino acids on subsequent bacterial deoxyribonucleic acid replication. J Bacteriol 92 : 609 617.
5. Boulton, C.A. (1989) Extracellular microbial lipids. In Microbial Lipids, Vol. 2. Ratledge, C. Wilkinson, S.G. (eds). London, UK : Academic Press, pp. 669 694.
6. Bozzi, M., Mignogna, G., Stefanini, S., Barra, D., Longhi, C., Valenti, P. Chiancone, E. (1997) A novel non-heme iron-binding ferritin related to the DNA-binding proteins of the Dps family in Listeria innocua. J Biol Chem 272 : 3259 3265.
7. Bradford, M.M. (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72 : 248 254.
8. Brady, S.F. Clardy, J. (2000) Long-chain N-acyl amino acid antibiotics isolated from heterologously expressed environmental DNA. J Am Chem Soc 122 : 12903 12904.
9. Brady, S.F. Clardy, J. (2005) N-acyl derivatives of arginine and tryptophan isolated from environmental DNA expressed in Escherichia coli. Org Lett 7 : 3613 3616.
10. Brady, S.F., Chao, C.J. Clardy, J. (2004) Long-chain N-acyltyrosine synthases from environmental DNA. Appl Environ Microbiol 70 : 6865 6870.
11. Brentjens, R.J., Ketterer, M., Apicella, M.A. Spinola, S.M. (1996) Fine tangled pili expressed by Haemophilus ducreyi are a novel class of pili. J Bacteriol 178 : 808 816.
12. Ceci, P., Ilari, A., Falvo, E., Giangiacomo, L. Chiancone, E. (2005) Reassessment of protein stability, DNA binding, and protection of Mycobacterium smegmatis Dps. J Biol Chem 280 : 34776 34785.
13. Claridge, C.A., Gourevitch, A. Lein, J. (1960) Bacterial penicillin amidase. Nature 187 : 237 238.
14. De Long, E.F. (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89 : 5685 5689.
15. Deutsch, D.G. Chin, S.A. (1993) Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist. Biochem Pharmacol 46 : 791 796.
16. Felton, G.W. Duffey, S.S. (1991) Reassessment of the role of gut alkalinity and detergency in insect herbivory. J Chem Ecol 17 : 1821 1836.
17. Görgen, G., Boland, W., Preiss, U. Simon, H. (1989) Synthesis of chiral 12-phenyldodecanoic acids - useful metabolic probes for the biosynthesis of 1-alkenes from fatty acids. Helv Chim Acta 72 : 917 928.
18. Grant, R.A., Filman, D.J., Finkel, S.E., Kolter, R. Hogle, J.M. (1998) The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat Struct Biol 5 : 294 303.
19. Gupta, S. Chatterji, D. (2003) Bimodal protection of DNA by Mycobacterium smegmatis DNA-binding protein from stationary phase cells. J Biol Chem 278 : 5235 5241.
20. Halitschke, R., Schittko, U., Pohnert, G., Boland, W. Baldwin, I.T. (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125 : 711 717.
21. Hébraud, M. Guzzo, J. (2000) The main cold shock protein of Listeria monocytogenes belongs to the family of ferritin-like proteins. FEMS Microbiol Lett 190 : 29 34.
22. Holt, J.G., Krieg, N.R., Sneath, P.H., Staley, J.T. Williams, S.T. (1993) Bergey's Manual of Determinative Bacteriology. Baltimore, MD, USA : Williams & Wilkins.
23. Irr, J.D. (1972) Control of nucleotide metabolism and ribosomal ribonucleic-acid synthesis during nitrogen starvation of Escherichia coli. J Bacteriol 110 : 554 561.
24. Kawai, Y., Yano, I. Kaneda, K. (1988) Various kinds of lipoamino acids including a novel serine-containing lipid in an opportunistic pathogen flavobacterium - their structures and biological activities on erythrocytes. Eur J Biochem 171 : 73 80.
25. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F. Hopwood, D.A. (eds) (2000) Practical Streptomyces Genetics. Norwich, UK : John Innes Foundation.
26. Lait, C.G., Alborn, H.T., Teal, P.E.A. Tumlinson, J.H. (2003) Rapid biosynthesis of N-linolenoyl-l-glutamine, an elicitor of plant volatiles, by membrane-associated enzyme(s) in Manduca sexta. Proc Natl Acad Sci USA 100 : 7027 7032.
27. Liu, X. Theil, E.C. (2005) Ferritins: dynamic management of biological iron and oxygen chemistry. Acc Chem Res 38 : 167 175.
28. McDaniel, R., Ebert-Khosla, S., Hopwood, D.A. Khosla, C. (1993) Engineered biosynthesis of novel polyketides. Science 262 : 1546 1550.
29. Maffei, M., Bossi, S., Spiteller, D., Mithöfer, A. Boland, W. (2004) Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol 134 : 1752 1762.
30. Mattiacci, L., Dicke, M. Posthumus, M.A. (1995) Beta-glucosidase - an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proc Natl Acad Sci USA 92 : 2036 2040.
31. Mithöfer, A., Müller, B., Wanner, G. Eichacker, L.A. (2002) Identification of defence-related cell wall proteins in Phytophthora sojae-infected soybean roots by ESI-MS/MS. Mol Plant Pathol 3 : 163 166.
32. Mori, N., Alborn, H.T., Teal, P.E.A. Tumlinson, J.H. (2001) Enzymatic decomposition of elicitors of plant volatiles in Heliothis virescens and Helicoverpa zea. J Insect Physiol 47 : 749 757.
33. Munford, R.S. Hunter, J.P. (1992) Acyloxyacyl hydrolase, a leukocyte enzyme that deacylates bacterial lipopolysaccharides, Has phospholipase, lysophospholipase, diacylglycerollipase, and acyltransferase activities in vitro. J Biol Chem 267 : 10116 10121.
34. Papinutto, E., Dundon, W.G., Pitulis, N., Battistutta, R., Montecucco, C. Zanotti, G. (2002) Structure of two iron-binding proteins from Bacillus anthracis. J Biol Chem 277 : 15093 15098.
35. Paré, P.W., Alborn, H.T. Tumlinson, J.H. (1998) Concerted biosynthesis of an insect elicitor of plant volatiles. Proc Natl Acad Sci USA 95 : 13971 13975.
36. Ping, L. (2004) Biosynthese von N-Acylglutaminen im Insektendarm: Beteiligung und Charakterisierung bakterieller Enzyme. Jena, Germany : Friedrich Schiller University.
37. van Poecke, R.M.P. Dicke, M. (2004) Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant. Plant Biol 6 : 387 401.
38. Pohnert, G., Jung, V., Haukioja, E., Lempa, K. Boland, W. (1999a) New fatty acid amides from regurgitant of lepidopteran (Noctuidae, Geometridae) caterpillars. Tetrahedron 55 : 11275 11280.
39. Pohnert, G., Koch, T. Boland, W. (1999b) Synthesis of volicitin: a novel three-component Wittig approach to chiral 17-hydroxylinolenic acid. Chem Commun 12 : 1087 1088.
40. Pulliainen, A.T., Haataja, S., Kahkonen, S. Finne, J. (2003) Molecular basis of H2O2 resistance mediated by streptococcal Dpr - demonstration of the functional involvement of the putative ferroxidase center by site-directed mutagenesis in Streptococcus suis. J Biol Chem 278 : 7996 8005.
41. Rainey, F., Weiss, N., Prauser, H. Stackebrandt, E. (1994) Further evidence for the phylogenetic coherence of Actinomycetes with group B-peptidoglycan and evidence for the phylogenetic intermixing of the genera Microbacterium and Aureobacterium as determined by 16s rDNA analysis. FEMS Microbiol Lett 118 : 135 139.
42. Ren, B., Tibbelin, G., Kajino, T., Asami, O. Ladenstein, R. (2003) The multi-layered structure of Dps with a novel di-nuclear ferroxidase center. J Mol Biol 329 : 467 477.
43. Schmid, P.C., Zuzarte-Augustin, M.L. Schmid, H.H.O. (1985) Properties of rat-liver N-acylethanolamine amidohydrolase. J Biol Chem 260 : 4145 4149.
44. Shevchenko, A., Wilm, M., Vorm, O. Mann, M. (1996) Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal Chem 68 : 850 858.
45. Spiteller, D. Boland, W. (2003) N-(17-acyloxy-acyl)-glutamines: novel surfactants from oral secretions of lepidopteran larvae. J Org Chem 68 : 8743 8749.
46. Spiteller, D., Dettner, K. Boland, W. (2000) Gut bacteria may be involved in interactions between plants, herbivores and their predators: microbial biosynthesis of N-acylglutamine surfactants as elicitors of plant volatiles. Biol Chem 381 : 755 762.
47. Spiteller, D., Oldham, N.J. Boland, W. (2004) N-(17- phosphonooxylinolenoyl) glutamine and N-(17-phosphonooxylinoleoyl)glutamine from insect gut: the first backbone-phosphorylated fatty acid derivatives in nature. J Org Chem 69 : 1104 1109.
48. Tate, R., Ferraioli, S., Filosa, S., Cermola, M., Riccio, A., Iaccarino, M. Patriarca, E.J. (2004) Glutamine utilization by Rhizobium etli. Mol Plant Microbe Interact 17 : 720 728.
49. Teneberg, S., MillerPodraza, H., Lampert, H.C., Evans, D.J., Evans, D.G., Danielsson, D. Karlsson, K.A. (1997) Carbohydrate binding specificity of the neutrophil-activating protein of Helicobacter pylori. J Biol Chem 272 : 19067 19071.
50. Tonello, F., Dundon, W.G., Satin, B., Molinari, M., Tognon, G., Grandi, G., et al. (1999) The Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure. Mol Microbiol 34 : 238 246.
51. Trivedi, O.A., Arora, P., Sridharan, V., Tickoo, R., Mohanty, D. Gokhale, R.S. (2004) Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 428 : 441 445.
52. Wittgren, B., Borgström, J., Piculell, L. Wahlund, K.G. (1998) Conformational change and aggregation of kappa-carrageenan studied by flow field-flow fractionation and multiangle light scattering. Biopolymers 45 : 85 96.
53. Yagi, H., Corzo, G. Nakahara, T. (1997) N-acyl amino acid biosynthesis in marine bacterium, Deleya marina. Biochim Biophys Acta-Ge Subj 1336 : 28 32.
54. Zhao, G.H., Ceci, P., Ilari, A., Giangiacomo, L., Laue, T.M., Chiancone, E. Chasteen, N.D. (2002) Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells - a ferritin-like DNA-binding protein of Escherichia coli. J Biol Chem 277 : 27689 27696.