Functional dissection of surfactin synthetase initiation module reveals insights into the mechanism of lipoinitiation

Chemistry and Biology

Volumn 17, Issue 8, 2010, Pages 872-880

  Kraas, Femke I ^a   Helmetag, Verena ^a   Wittmann, Melanie ^a   Strieker, Matthias ^a,b   Marahiel, Mohamed A ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

CHEMBIO

Indexed keywords

3 HYDROXYMYRISTIC ACID; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BETA-HYDROXYMYRISTIC ACID; LIPOPEPTIDE; LONG CHAIN FATTY ACID COENZYME A LIGASE; MYRISTIC ACID DERIVATIVE; PEPTIDE SYNTHASE; SURFACTIN SYNTHETASE;

ARTICLE; BACILLUS SUBTILIS; BIOCATALYSIS; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ANTI-BACTERIAL AGENTS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOCATALYSIS; COENZYME A LIGASES; LIPOPEPTIDES; MYRISTIC ACIDS; PEPTIDE SYNTHASES; PROTEIN STRUCTURE, TERTIARY;

BACILLUS SUBTILIS;

EID: 77956013672     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2010.06.015     Document Type: Article

References (55)

1. K. Arima, A. Kakinuma, and G. Tamura Surfactin, a crystalline peptidelipid surfactant produced by Bacillus subtilis: isolation, characterization and its inhibition of fibrin clot formation Biochem. Biophys. Res. Commun. 31 1968 488 494
2. C.J. Balibar, F.H. Vaillancourt, and C.T. Walsh Generation of D amino acid residues in assembly of arthrofactin by dual condensation/epimerization domains Chem. Biol. 12 2005 1189 1200
3. R.H. Baltz, V. Miao, and S.K. Wrigley Natural products to drugs: daptomycin and related lipopeptide antibiotics Nat. Prod. Rep. 22 2005 717 741
4. P.J. Belshaw, C.T. Walsh, and T. Stachelhaus Aminoacyl-CoAs as probes of condensation domain selectivity in nonribosomal peptide synthesis Science 284 1999 486 489
5. P.N. Black, Q. Zhang, J.D. Weimar, and C.C. DiRusso Mutational analysis of a fatty acyl-coenzyme A synthetase signature motif identifies seven amino acid residues that modulate fatty acid substrate specificity J. Biol. Chem. 272 1997 4896 4903
6. M. Blecher Synthesis of long-chain fatty acyl-coA thioesters using N-hydroxysuccinimide esters Methods Enzymol. 72 1981 404 408
7. J.M. Bonmatin, O. Laprevote, and F. Peypoux Diversity among microbial cyclic lipopeptides: iturins and surfactins. Activity-structure relationships to design new bioactive agents Comb. Chem. High Throughput Screen 6 2003 541 556
8. X. Cao, A.H. Wang, R.Z. Jiao, C.L. Wang, D.Z. Mao, L. Yan, and B. Zeng Surfactin induces apoptosis and G(2)/M arrest in human breast cancer MCF-7 cells through cell cycle factor regulation Cell Biochem. Biophys. 55 2009 163 171
9. P. Cosmina, F. Rodriguez, F. de Ferra, G. Grandi, M. Perego, G. Venema, and D. van Sinderen Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis Mol. Microbiol. 8 1993 821 831
10. V. De Crecy-Lagard, P. Marliere, and W. Saurin Multienzymatic non ribosomal peptide biosynthesis: identification of the functional domains catalysing peptide elongation and epimerisation C. R. Acad. Sci. III 318 1995 927 936
11. S. Doekel, and M.A. Marahiel Dipeptide formation on engineered hybrid peptide synthetases Chem. Biol. 7 2000 373 384
12. M.A. Fischbach, J.R. Lai, E.D. Roche, C.T. Walsh, and D.R. Liu Directed evolution can rapidly improve the activity of chimeric assembly-line enzymes Proc. Natl. Acad. Sci. USA 104 2007 11951 11956
13. S. Fuma, Y. Fujishima, N. Corbell, C. D'Souza, M.M. Nakano, P. Zuber, and K. Yamane Nucleotide sequence of 5′ portion of srfA that contains the region required for competence establishment in Bacillus subtilus Nucleic Acids Res. 21 1993 93 97
14. H. Heerklotz, and J. Seelig Leakage and lysis of lipid membranes induced by the lipopeptide surfactin Eur. Biophys. J. 36 2007 305 314
15. M. Hiramoto, K. Okada, S. Nagai, and H. Kawamoto The structure of viscosin, a peptide antibiotic. I. Syntheses of D- and L-3-hydroxyacyl-L-leucine hydrazides related to viscosin Chem. Pharm. Bull. (Tokyo) 19 1971 1308 1314
16. M. Juguet, S. Lautru, F.X. Francou, S. Nezbedova, P. Leblond, M. Gondry, and J.L. Pernodet An iterative nonribosomal peptide synthetase assembles the pyrrole-amide antibiotic congocidine in Streptomyces ambofaciens Chem. Biol. 16 2009 421 431
17. A. Kakinuma, A. Ouchida, T. Shima, H. Sugino, M. Isono, G. Tamura, and K. Arima Confirmation of the structure of surfactin by mass spectrometry Agric. Biol. Chem. 33 1969 1669 1671
18. Y. Kameda, K. Matsui, H. Kato, T. Yamada, and H. Sagai Antitumor activity of Bacillus natto. 3. Isolation and characterization of a cytolytic substance on Ehrlich ascites carcinoma cells in the culture medium of Bacillus natto KMD 1126 Chem. Pharm. Bull. (Tokyo) 20 1972 1551 1557
19. C. Klein, C. Kaletta, N. Schnell, and K.D. Entian Analysis of genes involved in biosynthesis of the lantibiotic subtilin Appl. Environ. Microbiol. 58 1992 132 142
20. A. Koglin, F. Lohr, F. Bernhard, V.V. Rogov, D.P. Frueh, E.R. Strieter, M.R. Mofid, P. Guntert, G. Wagner, and C.T. Walsh Structural basis for the selectivity of the external thioesterase of the surfactin synthetase Nature 454 2008 907 911
21. F. Kopp, U. Linne, M. Oberthur, and M.A. Marahiel Harnessing the chemical activation inherent to carrier protein-bound thioesters for the characterization of lipopeptide fatty acid tailoring enzymes J. Am. Chem. Soc. 130 2008 2656 2666
22. H. Kuwayama, S. Obara, T. Morio, M. Katoh, H. Urushihara, and Y. Tanaka PCR-mediated generation of a gene disruption construct without the use of DNA ligase and plasmid vectors Nucleic Acids Res. 30 2002 E2
23. S. Lautru, and G.L. Challis Substrate recognition by nonribosomal peptide synthetase multi-enzymes Microbiology 150 2004 1629 1636
24. S.G. Lee, and F. Lipmann Tyrocidine synthetase system Methods Enzymol. 43 1975 585 602
25. S. Lin, S.G. Van Lanen, and B. Shen A free-standing condensation enzyme catalyzing ester bond formation in C-1027 biosynthesis Proc. Natl. Acad. Sci. USA 106 2009 4183 4188
26. U. Linne, and M.A. Marahiel Control of directionality in nonribosomal peptide synthesis: role of the condensation domain in preventing misinitiation and timing of epimerization Biochemistry 39 2000 10439 10447
27. U. Linne, D.B. Stein, H.D. Mootz, and M.A. Marahiel Systematic and quantitative analysis of protein-protein recognition between nonribosomal peptide synthetases investigated in the tyrocidine biosynthetic template Biochemistry 42 2003 5114 5124
28. C.G. Marshall, M.D. Burkart, T.A. Keating, and C.T. Walsh Heterocycle formation in vibriobactin biosynthesis: alternative substrate utilization and identification of a condensed intermediate Biochemistry 40 2001 10655 10663
29. H. Matsuoka, K. Hirooka, and Y. Fujita Organization and function of the YsiA regulon of Bacillus subtilis involved in fatty acid degradation J. Biol. Chem. 282 2007 5180 5194
30. M. Menkhaus, C. Ullrich, B. Kluge, J. Vater, D. Vollenbroich, and R.M. Kamp Structural and functional organization of the surfactin synthetase multienzyme system J. Biol. Chem. 268 1993 7678 7684
31. H.D. Mootz, R. Finking, and M.A. Marahiel 4′-Phosphopantetheine transfer in primary and secondary metabolism of Bacillus subtilis J. Biol. Chem. 276 2001 37289 37298
32. H.D. Mootz, D. Schwarzer, and M.A. Marahiel Ways of assembling complex natural products on modular nonribosomal peptide synthetases ChemBioChem 3 2002 490 504
33. C.N. Mulligan Environmental applications for biosurfactants Environ. Pollut. 133 2005 183 198
34. M.M. Nakano, M.A. Marahiel, and P. Zuber Identification of a genetic locus required for biosynthesis of the lipopeptide antibiotic surfactin in Bacillus subtilis J. Bacteriol. 170 1988 5662 5668
35. E. Nissen, G. Pauli, J. Vater, and D. Vollenbroich Application of surfactin for mycoplasma inactivation in virus stocks In Vitro Cell. Dev. Biol. Anim. 33 1997 414 415
36. F. Peypoux, J.M. Bonmatin, and J. Wallach Recent trends in the biochemistry of surfactin Appl. Microbiol. Biotechnol. 51 1999 553 563
37. A. Powell, M. Borg, B. Amir-Heidari, J.M. Neary, J. Thirlway, B. Wilkinson, C.P. Smith, and J. Micklefield Engineered biosynthesis of nonribosomal lipopeptides with modified fatty acid side chains J. Am. Chem. Soc. 129 2007 15182 15191
38. C. Rausch, I. Hoof, T. Weber, W. Wohlleben, and D.H. Huson Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution BMC Evol. Biol. 7 2007 78
39. E.D. Roche, and C.T. Walsh Dissection of the EntF condensation domain boundary and active site residues in nonribosomal peptide synthesis Biochemistry 42 2003 1334 1344
40. S.A. Samel, G. Schoenafinger, T.A. Knappe, M.A. Marahiel, and L.O. Essen Structural and functional insights into a peptide bond-forming bidomain from a nonribosomal peptide synthetase Structure 15 2007 781 792
41. A. Schneider, and M.A. Marahiel Genetic evidence for a role of thioesterase domains, integrated in or associated with peptide synthetases, in non-ribosomal peptide biosynthesis in Bacillus subtilis Arch. Microbiol. 169 1998 404 410
42. D. Schwarzer, H.D. Mootz, U. Linne, and M.A. Marahiel Regeneration of misprimed nonribosomal peptide synthetases by type II thioesterases Proc. Natl. Acad. Sci. USA 99 2002 14083 14088
43. S.A. Sieber, and M.A. Marahiel Molecular mechanisms underlying nonribosomal peptide synthesis: approaches to new antibiotics Chem. Rev. 105 2005 715 738
44. T. Stachelhaus, H.D. Mootz, V. Bergendahl, and M.A. Marahiel Peptide bond formation in nonribosomal peptide biosynthesis. Catalytic role of the condensation domain J. Biol. Chem. 273 1998 22773 22781
45. S. Steller, A. Sokoll, C. Wilde, F. Bernhard, P. Franke, and J. Vater Initiation of surfactin biosynthesis and the role of the SrfD-thioesterase protein Biochemistry 43 2004 11331 11343
46. M. Strieker, and M.A. Marahiel The structural diversity of acidic lipopeptide antibiotics ChemBioChem 10 2009 607 616
47. M. Strieker, F. Kopp, C. Mahlert, L.O. Essen, and M.A. Marahiel Mechanistic and structural basis of stereospecific Cbeta-hydroxylation in calcium-dependent antibiotic, a daptomycin-type lipopeptide ACS Chem. Biol. 2 2007 187 196
48. Z. Suo Thioesterase portability and peptidyl carrier protein swapping in yersiniabactin synthetase from Yersinia pestis Biochemistry 44 2005 4926 4938
49. C.C. Tseng, S.D. Bruner, R.M. Kohli, M.A. Marahiel, C.T. Walsh, and S.A. Sieber Characterization of the surfactin synthetase C-terminal thioesterase domain as a cyclic depsipeptide synthase Biochemistry 41 2002 13350 13359
50. N. Tsukagoshi, G. Tamura, and K. Arima A novel protoplast-bursting factor (surfactin) obtained from bacillus subtilis IAM 1213. II. The interaction of surfactin with bacterial membranes and lipids Biochim. Biophys. Acta 196 1970 211 214
51. J. Vater, T. Stein, D. Vollenbroich, V. Kruft, B. Wittmann-Liebold, P. Franke, L. Liu, and P. Zuber The modular organization of multifunctional peptide synthetases J. Protein Chem. 16 1997 557 564
52. D. Vollenbroich, M. Ozel, J. Vater, R.M. Kamp, and G. Pauli Mechanism of inactivation of enveloped viruses by the biosurfactant surfactin from Bacillus subtilis Biologicals 25 1997 289 297
53. C.T. Walsh, and M.A. Fischbach Natural products version 2.0: connecting genes to molecules J. Am. Chem. Soc. 132 2010 2469 2493
54. M. Wittmann, U. Linne, V. Pohlmann, and M.A. Marahiel Role of DptE and DptF in the lipidation reaction of daptomycin FEBS J. 275 2008 5343 5354
55. E. Yeh, R.M. Kohli, S.D. Bruner, and C.T. Walsh Type II thioesterase restores activity of a NRPS module stalled with an aminoacyl-S-enzyme that cannot be elongated ChemBioChem 5 2004 1290 1293