The Pseudomonas aeruginosa antimetabolite L -2-amino-4-methoxy-trans-3-butenoic acid (AMB) is made from glutamate and two alanine residues via a thiotemplate-linked tripeptide precursor

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Murcia, Nelson Rojas ^a   Lee, Xiaoyun ^a   Waridel, Patrice ^a   Maspoli, Alessandro ^a   Imker, Heidi J ^b,c   Chai, Tiancong ^a   Walsh, Christopher T ^b   Reimmann, Cornelia ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Oxyvinylglycine; Pseudomonas; Secondary metabolite; Thiotemplate; Toxin

Indexed keywords

2 AMINO 4 METHOXY TRANS 3 BUTENOIC ACID; ADENOSINE TRIPHOSPHATE; ALANINE; ALLYLGLYCINE; ANTIMETABOLITE; BACTERIAL TOXIN; DNA FRAGMENT; GLUTAMIC ACID; PLASMID DNA; PYROPHOSPHATE; TRIPEPTIDE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINOACYLATION; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOINFORMATICS; CELL LYSATE; DNA SEQUENCE; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC MANIPULATION; MASS SPECTROMETRY; MICROCYSTIS AERUGINOSA; NONHUMAN; NONRIBOSOMAL PEPTIDE SYNTHESIS; PHYLOGENY; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN ACETYLATION; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA;

EUKARYOTA; PROKARYOTA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 84926681329     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00170     Document Type: Article

References (53)

1. Bachmann, B. O., and Ravel, J. (2009). Methods for in silico prediction of microbial secondary metabolic pathways from DNA sequence data. Methods Enzymol. 458, 181-217. doi: 10.1016/S0076-6879(09)04808-3
2. Banowetz, G. M., Azevedo, M. D., Armstrong, D. J., Halgren, A. B., and Mills, D. I. (2008). Germination arrest factor (GAF): biological properties of a novel, naturally-occurring herbicide produced by selected isolates of rhizosphere bacteria. Biol. Control 46, 380-390. doi: 10.1016/j.biocontrol.2008.04.016
3. Berkowitz, D., Charrette, B. D., Karukurichi, K. R., and McFadden, J. M. (2006). a-Vinylic amino acids: occurrence, asymmetric synthesis, and biochemical mechanisms. Tetrahedron Asymmetry 17, 869-882. doi: 10.1016/j.tetasy.2006.02.026
4. Boc, A., Diallo, A. B., and Makarenkov, V. (2012). T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res. 40, W573-W579. doi: 10.1093/nar/gks485
5. Cornell, N. W., Zuurendonk, P. F., Kerich, M. J., and Straight, C. B. (1984). Selective inhibition of alanine aminotransferase and aspartate aminotransferase in rat hepatocytes. J. Biochem. 220, 707-716.
6. Dashman, T., and Kamm, J. J. (1979). Inhibition of d-aminolevulinic acid synthetase and d-aminolevulinic acid dehydrase by L-2-amino-4-methoxy-trans-3-butenoic acid in the rat. Life Sci. 24, 185-192. doi: 10.1016/0024-3205(79)90129-2
7. Dorrestein, P., Blackhall, J., Straight, P., Fischbach, M., Garneau-Tsodikova, S., Edwards, D.,et al. (2006). Activity screening of carrier domains within nonribosomal peptide synthetases using complex substrate mixtures and large molecule mass spectrometry. Biochemistry 45, 1537-1546. doi: 10.1021/bi052333k
8. Farinha, M. A., and Kropinski, A. M. (1990). High efficiency electroporation of Pseudomonas aeruginosa using frozen cell suspensions. FEMS Microbiol. Lett. 58, 221-225. doi: 10.1016/S0378-1097(05)80043-6
9. Fernández, M., Cuadrado, Y., Aparicio, J. F., and Martín, J. F. (2004). Role of homoserine and threonine pathway intermediates as precursors for the biosynthesis of aminoethoxyvinylglycine in Streptomyces sp. NRRL 5331. Microbiology 50, 1467-1474. doi: 10.1099/mic.0.26851-0
10. Halgren, A., Maselko, M., Azevedo, M., Mills, D., Armstrong, D., and Banowetz, G. (2013). Genetics of germination-arrest factor (GAF) production by Pseudomonas fluorescens WH6: identification of a gene cluster essential for GAF biosynthesis. Microbiology 159, 36-45. doi: 10.1099/mic.0.062166-0
11. Hausinger, R. (2004). Fe(II)/a-ketoglutarate-dependent hydroxylases and related enzymes. Crit. Rev. Biochem. Mol. Biol. 39, 21-68. doi: 10.1080/10409230490440541
12. Hirata, H., Kato, A., Nakatani, S., Aiba, T., Oohashi, Y., and Goto, M. (1993). Antibiotics WAP-5044C and WAP-5044A, WAP-5044C derivative, their manufactures with Streptomyces, and fungicides containing them. JP Patent 05105657.
13. Hollenhorst, M., Bumpus, S., Matthews, M., Bollinger, J. Jr., Kelleher, N., and Walsh, C. (2010). The nonribosomal peptide synthetase enzyme DdaD tethers Nß-Fumaramoyl-l-2,3-diaminopropionate for Fe(II)/a-ketoglutarate-dependent epoxidation by DdaC during dapdiamide antibiotic biosynthesis. J. Am. Chem. Soc. 132, 15773-15781. doi: 10.1021/ja1072367
14. Lee, X., Azevedo, M., Armstrong, D., Banowetz, G., and Reimmann, C. (2013a). The Pseudomonas aeruginosa antimetabolite L-2-amino-4-methoxy-trans-3-butenoic acid inhibits growth of Erwinia amylovora and acts as a seed germination-arrest factor. Environ. Microbiol. Rep. 5, 83-89. doi: 10.1111/j.1758-2229.2012.00395.x
15. Lee, J., Wu, J., Deng, Y., Wang, J., Wang, C., Wang, J.,et al. (2013b). A cell-cell communication signal integrates quorum sensing and stress response. Nat. Chem. Biol. 9, 339-343. doi: 10.1038/nchembio.1225
16. Lee, X., Fox, A., Sufrin, J., Henry, H., Majcherczyk, P., Haas, D.,et al. (2010). Identification of the biosynthetic gene cluster for the Pseudomonas aeruginosa antimetabolite L-2-Amino-4-methoxy-trans-3-butenoic acid. J. Bacteriol. 192, 4251-4255. doi: 10.1128/JB.00492-10
17. Lee, X., Reimmann, C., Greub, G., Sufrin, J., and Croxatto, A. (2012). The Pseudomonas aeruginosa toxin L-2-Amino-4-methoxy-trans-3-butenoic acid inhibits growth and induces encystment in Acanthamoeba castellanii. Microbes Infect. 14, 268-272. doi: 10.1016/j.micinf.2011.10.004
18. Lyczak, J. B., Cannon, C. L., and Pier, G. B. (2002). Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15, 194-222. doi: 10.1128/CMR.15.2.194-222.2002
19. Marahiel, M. A., Stachelhaus, T., and Mootz, H. D. (1997). Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97, 2651-2674. doi: 10.1021/cr960029e
20. Marchler-Bauer, A., and Bryant, S. H. (2004). CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 32, 327-331. doi: 10.1093/nar/gkh454
21. Matoo, A. K., Anderson, J. D., Chalutz, E., and Lieberman, M. (1979). Influence of enol ether amino acids, inhibitors of ethylene biosynthesis, on aminoacyl transfer RNA synthetases and protein synthesis. Plant Physiol. 64, 289-292. doi: 10.1104/pp.64.2.289
22. McPhail, K. L., Armstrong, D. J., Azevedo, M. D., Banowetz, G. M., and Mills, D. I. (2010). 4-Formylaminooxyvinylglycine, an herbicidal germination-arrest factor from Pseudomonas rhizosphere bacteria. J. Nat. Prod. 73, 1853-1857. doi: 10.1021/np1004856
23. Meier, J., Patel, A., Niessen, S., Meehan, M., Kersten, R., Yang, J.,et al. (2011). Practical 4'-phosphopantetheine active site discovery from proteomic samples. J. Proteome Res. 10, 320-329. doi: 10.1021/pr100953b
24. Meluzzi, D., Zheng, W., Hensler, M., Nizet, V., and Dorrestein, P. (2008). Top-down mass spectrometry on low-resolution instruments: characterization of phosphopantetheinylated carrier domains in polyketide and non-ribosomal biosynthetic pathways. Bioorg. Med. Chem. Lett. 18, 3107-3111. doi: 10.1016/j.bmcl.2007.10.104
25. Metcalf, W. W., and van der Donk, W. A. (2009). Biosynthesis of phosphonic and phosphinic acid natural products. Annu. Rev. Biochem. 78, 65-94. doi: 10.1146/annurev.biochem.78.091707.100215
26. Miles, E. W. (1975). A new type of pyridoxal-p enzyme catalyzed reaction: the conversion of β, γ-unsaturated amino acids to saturated a-keto acids by tryptophan synthase. Biochem. Biophys. Res. Commun. 66, 94-102. doi: 10.1016/S0006-291X(75)80299-3
27. Mitchell, R. E., and Coddington, J. M. (1991). Biosynthetic pathway to rhizobitoxine in Pseudomonas andropogonis. Phytochemistry 30, 1809-1814. doi: 10.1016/0031-9422(91)85018-U
28. Mitchell, R. E., Frey, E. J., and Benn, M. H. (1986). Rhizobitoxin and L-threohydroxythreonine production by the plant pathogen Pseudomonas andropogonis. Phytochemistry 25, 2711-2715.
29. Owens, L. D., Thompson, J. F., Pitcher, R. G., and Williams, T. (1972). Structure of rhizobitoxine, an antimetabolic enolether amino-acid from Rhizobium japonicum. J. Chem. Soc. Chem. Commun. (Camb.) 12, 714. doi: 10.1039/c39720000714
30. Pruess, D. L., Scannell, J. P., Kellett, M., Ax, H. A., Janecek, J., Williams, T. H.,et al. (1974). Antimetabolites produced by microorganisms. X. L-2-Amino-4-(2-aminoethoxy)-trans-3-butenoic acid. J. Antibiot. 27, 229-233. doi: 10.7164/antibiotics.27.229
31. Rando, R. R. (1974). β,γ-Unsaturated amino acids as irreversible enzyme inhibitors. Nature 250, 586-587. doi: 10.1038/250586a0
32. Rando, R. R., Relyea, N., and Cheng, L. (1976). Mechanism of the irreversible inhibition of aspartate aminotransferase by the bacterial toxin L-2-Amino-4-methoxy-trans-3-butenoic acid. J. Biol. Chem. 251, 3306-3312.
33. Sahm, U., Knobloch, G., and Wagner, F. (1973). Isolation and characterization of the methionine antagonist L-2-amino-4-methoxy-trans-3-butenoic acid from Pseudomonas aeruginosa grown on n-paraffin. J. Antibiot. 26, 389-390. doi: 10.7164/antibiotics.26.389
34. Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
35. Sambrook, J., and Russell, D. (2001). Molecular Cloning: A Laboratory Manual, 3rd Edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
36. Scannell, J. P., Pruess, D. L., Demny, T. C., Sello, L. H., Williams, T., and Stempel, A. (1972). Antimetabolites produced by microorganisms. V. L-2-Amino-4-methoxy-trans-3-butenoic acid. J. Antibiot. 25, 122-127. doi: 10.7164/antibiotics.25.122
37. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W.,et al. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7, 539. doi: 10.1038/msb.2011.75
38. Smith, S. B., and Freeland, R. A. (1981). Functional inhibition of cytosolic and mitochondrial aspartate aminotransferase by L-2-amino-4-methoxy-trans-3-butanoic acid in isolated rat hepatocytes and mitochondria. Arch. Biochem. Biophys. 209, 335-341. doi: 10.1016/0003-9861(81)90289-7
39. Stachelhaus, T., Mootz, H. D., Bergendahl, V., and Marahiel, M. A. (1998). Peptide bond formation in nonribosomal peptide biosynthesis. Catalytic role of the condensation domain. J. Biol. Chem. 273, 22773-22781. doi: 10.1074/jbc.273.35.22773
40. Stanisich, V. A., and Holloway, B. W. (1972). A mutant sex factor of Pseudomonas aeruginosa. Genet. Res. 19, 91-108. doi: 10.1017/S0016672300014294
41. Stein, T., Vater, J., Kruft, V., Otto, A., Wittmann-Liebold, B., Franke, P.,et al. (1996). The multiple carrier model of nonribosomal peptide biosynthesis at modular multienzymatic templates. J. Biol. Chem. 271, 15428-15435. doi: 10.1074/jbc.271.26.15428
42. Tatum, E. L., and Lederberg, J. (1947). Gene recombination in the bacterium. J. Bacteriol. 53, 673-684.
43. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680. doi: 10.1093/nar/22.22.4673
44. Tillet, D., Dittmann, E., Erhard, M., von Döhren, H., and Neilan, B. A. (2000). Structural orgnization of microcystin biosynthesis in Mycrocystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem. Biol. 216, 255-265.
45. Tisdale, M. J. (1981). The effect of L-2-amino-4-methoxy-trans-3-butenoic acid on serine hydroxymethyl transferase. Chem. Biol. Interact. 34, 75-83. doi: 10.1016/0009-2797(81)90092-2
46. Voisard, C., Rella, M., and Haas, D. (1988). Conjugative transfer of plasmid RP1 to soil isolates of Pseudomonas fluorescens is facilitated by certain large RP1 deletions. FEMS Microbiol. Lett. 55, 9-13. doi: 10.1111/j.1574-6968.1988.tb02790.x
47. Vrljic, M., Sahm, H., and Eggeling, L. (1996). A new type of transporter with a new type of cellular function: L-lysine export from Corynebacterium glutamicum. Mol. Microbiol. 22, 815-826. doi: 10.1046/j.1365-2958.1996.01527.x
48. Winsor, G. L., Lam, D. K., Fleming, L., Lo, R., Whiteside, M. D., Yu, N. Y.,et al. (2011). Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39, D596-D600. doi: 10.1093/nar/gkq869
49. Yasuta, T., Okazaki, S., Mitsui, H., Yuhashi, K., Ezura, H., and Minamisawa, K. (2001). DNA sequence and mutational analysis of rhizobotoxin biosynthesis genes in Bradyrhizobium elkanii. Appl. Environ. Microbiol. 67, 4999-5009. doi: 10.1128/AEM.67.11.4999-5009.2001
50. Ye, L., Cornelis, P., Guillemyn, K., Ballet, S., Christophersen, C., and Hammerich, O. (2014). Structure revision of N-Mercapto-4-formylcarbostyril produced by Pseudomonas fluorescens G308 to 2-(2-Hydroxyphenyl)thiazole-4-carbaldehyde [aeruginaldehyde]. Nat. Prod. Commun. 9, 789-794.
51. Ye, R. W., Haas, D., Ka, J. O., Krishnapillai, V., Zimmermann, A., Baird, C.,et al. (1995). Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. J. Bacteriol. 177, 3606-3609.
52. Yin, J., Lin, A. J., Golan, D. E., and Walsh, C. T. (2006). Site-specific protein labeling by Sfp phosphopantetheinyl transferase. Nat. Protoc. 1, 280-285. doi: 10.1038/nprot.2006.43
53. Youard, Z. A., Wenner, N., and Reimmann, C. (2011). Iron acquisition with the natural siderophore enantiomers pyochelin and enantio-pyochelin in Pseudomonas species. Biometals 24, 513-522. doi: 10.1007/s10534-010-9399-9