Importance of the long-chain fatty acid beta-hydroxylating cytochrome P450 Enzyme YbdT for lipopeptide biosynthesis in Bacillus subtilis strain OKB105

International Journal of Molecular Sciences

Volumn 12, Issue 3, 2011, Pages 1767-1786

  Youssef, Noha H ^a   Wofford, Neil ^b   McInerney, Michael J ^b  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

Bacillus subtilis; Beta hydroxylation; Cytochrome P450; Long chain fatty acids; Surfactin; YbdT

Indexed keywords

3 HYDROXYMYRISTIC ACID; 3 HYDROXYMYRISTOYL COENZYME A; BIOSURFACTANT; COENZYME A; CYTOCHROME P450; HYDROXY FATTY ACID; LIPOPEPTIDE; LONG CHAIN FATTY ACID; MYRISTIC ACID DERIVATIVE; PROTEIN YBDT; SURFACTIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BETA-HYDROXYMYRISTIC ACID; CYCLOPEPTIDE; FATTY ACID; SURFACTIN PEPTIDE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL FREE SYSTEM; CHEMICAL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENE MUTATION; MASS SPECTROMETRY; NONHUMAN; PEPTIDE SYNTHESIS; WILD TYPE; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR WEIGHT; SITE DIRECTED MUTAGENESIS;

BACILLUS SUBTILIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CYTOCHROME P-450 ENZYME SYSTEM; FATTY ACIDS; LIPOPEPTIDES; MOLECULAR WEIGHT; MUTAGENESIS, SITE-DIRECTED; MYRISTIC ACIDS; PEPTIDES, CYCLIC;

EID: 79953327543     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms12031767     Document Type: Article

References (63)

1. Banat, I.M. Biosurfactants production and possible uses in microbial enhanced oil recovery and oil pollution remediation: a review. Bioresour. Technol. 1995, 51, 1-12.
2. Banat, I.M.; Makkar, R.S.; Cameotra, S.S. Potential commercial applications of microbial surfactants. Appl. Microbiol. Biotechnol. 2000, 53, 495-508.
3. Georgiou, G.; Lin, S.C.; Sharma, M.M. Surface-active compounds from microorganisms. Biotechnology 1999, 10, 60-65.
4. Ron, E.Z.; Rosenberg, E. Natural roles of biosurfactants. Environ. Microbiol. 2001, 3, 229-236.
5. Seydlová, G.; Svobodová, J. Review of surfactin chemical properties and the potential biomedical applications. Cent. Eur. J. Med. 2008, 3, 123-133.
6. Arima, K.; Kakinuma, A.; Tamura, G. Surfactin, a crystaline peptidelipid surfactant produced by Bacillus subtilis: Isolation, characterization, and its inhibition of fibrin clot formation. Biochem. Biophys. Res. Commun. 1968, 31, 488-497.
7. Grangemard, I.; Bonmatin, J.M.; Bernillon, J.; Das, B.C.; Peypoux, F. Lichenysins G, a novel family of lipopeptide biosurfactants from Bacillus licheniformis IM 1307: production, isolation and structural evaluation by NMR and mass spectrometry. J. Antibiot. 1999, 52, 363-373.
8. Jenny, K.; Käppeli, O.; Fiechter, A. Biosurfactants from Bacillus licheniformis: structural analysis and characterization. Appl. Microbiol. Biotechnol. 1991, 36, 5-13.
9. Peypoux, F.; Bonmatin, J.M.; Wallach, J. Recent trends in the biochemistry of surfactin. Appl. Microbiol. Biotechnol. 1999, 51, 553-563.
10. Marahiel, M.A.; Stachelhaus, T.; Mootz, H.D. Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 1997, 97, 2651-2674.
11. Rausch, C.; Hoof, I.; Weber, T.; Wohlleben, W.; Huson, D. Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution. BMC Evol. Biol. 2007, 7, 78.
12. Straight, P.D.; Fischbach, M.A.; Walsh, C.T.; Rudner, D.Z.; Kolter, R. A singular enzymatic megacomplex from Bacillus subtilis. Proc. Nat. Acad. Sci. USA 2007, 104, 305-310.
13. Strieker, M.; Tanović, A.; Marahiel, M.A. Nonribosomal peptide synthetases: structures and dynamics. Curr. Opin. Struct. Biol. 2010, 20, 234-240.
14. Walsh, C.T. Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 2004, 303, 1805-1810.
15. Bruner, S.D.; Weber, T.; Kohli, R.M.; Schwarzer, D.; Marahiel, M.A.; Walsh, C.T.; Stubbs, M.T. Structural basis for the cyclization of the lipopeptide antibiotic surfactin by the thioesterase domain SrfTE. Structure 2002, 10, 301-310.
16. Cosmina, P.; Rodriguez, F.; de Ferra, F.; Grandi, G.; Perego, M.; Venema, G.; van Sinderen, D. Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis. Mol. Microbiol. 1993, 8, 821-831.
17. D'Souza, C.; Nakano, M.M.; Corbell, N.; Zuber, P. Amino-acylation site mutations in amino acid-activating domains of surfactin synthetase: effects on surfactin production and competence development in Bacillus subtilis. J. Bacteriol. 1993, 175, 3502-3510.
18. Galli, G.; Rodriguez, F.; Cosmina, P.; Pratesi, C.; Nogarotto, R.; de Ferra, F.; Grandi, G. Characterization of the surfactin synthetase multi-enzyme complex. Biochim. Biophys. Acta 1994, 1205, 19-28.
19. Menkhaus, M.; Ullrich, C.; Kluge, B.; Vater, J.; Vollenbroich, D.; Kamp, R.M. Structural and functional organization of the surfactin synthetase multienzyme system. J. Biol. Chem. 1993, 268, 7678-7684.
20. Nakano, M.M.; Corbell, N.; Besson, J.; Zuber, P. Isolation and characterization of sfp: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis. Mol. Gen. Genet. 1992, 232, 313-321.
21. Vollenbroich, D.; Mehta, N.; Zuber, P.; Vater, J.; Kamp, R.M. Analysis of surfactin synthetase subunits in srfA mutants of Bacillus subtilis OKB105. J. Bacteriol. 1994, 176, 395-400.
22. Steller, S.; Sokoll, A.; Wilde, C.; Bernhard, F.; Franke, P.; Vater, J. Initiation of surfactin biosynthesis and the role of the SrfD-thioesterase protein. Biochemistry 2004, 43, 11331-11343.
23. Kraas, F.I.; Helmetag, V.; Wittmann, M.; Strieker, M.; Marahiel, M.A. Functional Dissection of Surfactin Synthetase Initiation Module Reveals Insights into the Mechanism of Lipoinitiation. Chem. Biol. 2010, 17, 872-880.
24. Bonmatin, J.M.; Genest, M.; Labbé, H.; Ptak, M. Solution three-dimensional structure of surfactin: A cyclic lipopeptide studied by 1H-NMR, distance geometry, and molecular dynamics. Biopolymers 1994, 34, 975-986.
25. Stachelhaus, T.; Marahiel, M.A. Rational design of peptide antibiotics by targeted replacement of bacterial and fungal domains. Science 1995, 269, 5571-5574.
26. Yakimov, M.M.; Fredrickson, H.L.; Timmis, K.N. Effect of heterogeneity of hydrophobic moieties on surface activity of lichenysin A, a lipopeptide biosurfactant from Bacillus licheniformis BAS50. Biotechnol. Appl. Biochem. 1996, 23, 13-18.
27. Schneider, A.; Stachelhaus, T.; Marahiel, M.A. Targeted alteration of the substrate specificity of peptide synthetases by rational module swapping. Mol. Gen. Genet. 1998, 257, 308-318.
28. Deleu, M.; Bouffioux, O.; Razafindralambo, H.; Paquot, M.; Hbid, C.; Thonart, P.; Jacques, P.; Brasseur, R. Interaction of Surfactin with Membranes: A Computational Approach. Langmuir 2003, 19, 3377-3385.
29. Youssef, N.H.; Duncan, K.E.; McInerney, M.J. Importance of 3-hydroxyfatty acid composition of lipopeptides for biosurfactant activity. Appl. Environ. Microbiol. 2005, 71, 7690-7695.
30. von Wachenfeldt, C.; Hedenrstedt, L. Respiratory cytochromes, other heme proteins, and heme biosynthesis. In Bacillus subtilis and Its Closest Relatives: from Genes to Cells; Sonenshein, A.L., Hoch, J.A., Losick, R., Eds.; ASM Press: Washington, DC, USA, 2002; pp. 163-180.
31. Hlavica, P.; Lehnerer, M. Oxidative biotransformation of fatty acids by cytochromes P450: Predicted key structural elements orchestrating substrate specificity, regioselectivity and catalytic efficiency. Curr. Drug Metabol. 2010, 11, 85-104.
32. Cryle, M.J.; Matovic, N.J.; de Voss, J.J. Products of Cytochrome P450BioI (CYP107H1)-Catalyzed Oxidation of Fatty Acids. Org. Lett. 2003, 5, 3341-3344.
33. Cryle, M.J.; Schlichting, I. Structural insights from a P450 Carrier Protein complex reveal how specificity is achieved in the P450BioI ACP complex. Proc. Natl. Acad. Sci. USA 2008, 105, 15696-15701.
34. Gustafsson, M.C.U.; Roitel, O.; Marshall, K.R.; Noble, M.A.; Chapman, S.K.; Pessegueiro, A.; Fulco, A.J.; Cheesman, M.R.; von Wachenfeldt, C.; Munro, A.W. Expression, purification, and characterization of Bacillus subtilis cytochromes P450 CYP102A2 and CYP102A3: Flavocytochrome homologues of P450 BM3 from Bacillus megaterium. Biochemistry 2004, 43, 5474-5487.
35. Reddick, J.J.; Antolak, S.A.; Raner, G.M. PksS from Bacillus subtilis is a cytochrome P450 involved in bacillaene metabolism. Biochem. Biophys. Res. Commun. 2007, 358, 363-367.
36. Rivolta, C.; Soldo, B.; Lazarevic, V.; Joris, B.; Mauel, C.; Karamat, D. A 35.7 kb DNA fragment from the Bacillus subtilis chromosome containing a putative 12.3 kb operon involved in hexuronate catabolism and a perfectly symmetrical hypothetical catabolite-responsive element. Microbiology 1998, 144, 877-884.
37. Belitsky, B.R.; Gustafsson, M.C.; Sonenshein, A.L.; von Wachenfeldt, C. An lrp-like gene of Bacillus subtilis involved in branched-chain amino acid transport. J. Bacteriol. 1997, 179, 5448-5457.
38. Cryle, M.J.; Bell, S.G.; Schlichting, I. Structural and biochemical characterization of the cytochrome P450 CypX (CYP134A1) from Bacillus subtilis: A cyclo-L-leucyl-L-leucyl dipeptide oxidase. Biochemistry 2010, 49, 7282-7296.
39. Matsunaga, I.; Ueda, A.; Fujiwara, N.; Sumimoto, T.; Ichihara, K. Characterization of the ybdT gene product of Bacillus subtilis: novel fatty acid beta-hydroxylating cytochrome P450. Lipids 1999, 34, 841-846.
40. Lee, D.-S.; Yamada, A.; Sugimoto, H.; Matsunaga, I.; Ogura, H.; Ichihara, K.; Adachi, S.-I.; Park, S.-Y.; Shiro, Y. Substrate recognition and molecular mechanism of fatty acid hydroxylation by cytochrome P450 from Bacillus subtilis. J. Biol. Chem. 2003, 278, 9761-9767.
41. Majewski, J.; Cohan, F.M. DNA sequence similarity requirements for interspecific recombination in Bacillus. Genetics 1999, 153, 1525-1533.
42. Zar, J.H. Two-sample hypotheses. In Biostatistical Analysis, 4th ed.; Ryu, T., Ed.; Pentice Hall: Upper Saddle River, NJ, USA, 1999; pp. 122-160.
43. Christie, W.W. The lipid library: Mass spectra of some miscellaneous fatty acids and other lipid derivatives-Archive. Avaiable online: http://lipidlibrary.aocs.org/ms/arch_xyz/index.htm#tmsa (accessed on 1 December 2010).
44. Christie, W.W. The AOCS lipid library: Methyl esters of fatty acids-Archive of mass spectra. Avaiable online: http://lipidlibrary.aocs.org/ms/arch_me/index.htm (accessed on 1 December 2010).
45. Christie, W.W. The AOCS lipid library: Mass spectra of methyl esters of fatty acids. Part 1. Normal saturated fatty acids. Avaiable online: http://lipidlibrary.aocs.org/ms/ms03/index.htm (accessed on 1 December 2010).
46. Chickos, J.S.; Way, B.A.; Wilson, J.; Shaharuzzaman, M.; Laird, J.; Landt, M. Analysis of 3-hydroxydodecanedioic acid for studies of fatty acid metabolic disorders: Preparation of stable isotope standards. J. Clin. Lab. Anal. 2002, 16, 115-120.
47. Peypoux, F.; Bonmatin, J.M.; Labbe, H.; Grangemard, I.; Das, B.C.; Ptak, M.; Wallach, J.; Michel, G. [Ala 4] surfactin, a novel isoform from Bacillus subtilis studied by mass and NMR spectroscopies. Eur. J. Biochem. 1994, 224, 89-96.
48. Kowall, M.; Vater, J.; Kluge, B.; Stein, T.; Franke, P.; Ziessow, D. Separation and characterization of surfactin isoforms produced by Bacillus subtilis OKB 105. J. Colloid Interface Sci. 1998, 204, 1-8.
49. Bonmatin, J.-M.; Labbe, H.; Grangemard, I.; Peypoux, F.; Maget-Dana, R.; Ptak, M.; Michel, G. Production, isolation and characterization of [Leu4]- and [Ile4]-surfactins from Bacillus subtilis. Lett. Pept. Sci. 1995, 2, 41-47.
50. Tang, J.-S.; Zhao, F.; Gao, H.; Dai, Y.; Yao, Z.-H.; Hong, K.; Li, J.; Ye, W.-C.; Yao, X.-S. Characterization and Online Detection of Surfactin Isomers Based on HPLC-MSn Analyses and Their Inhibitory Effects on the Overproduction of Nitric Oxide and the Release of TNF-OE± and IL-6 in LPS-Induced Macrophages. Mar. Drugs 2010, 8, 2605-2618.
51. Morikawa, M.; Hirata, Y.; Imanaka, T. A study on the structure-function relationship of lipopeptide biosurfactants. Biochim. Biophys. Acta 2000, 1488, 211-218.
52. Ingham, C.J.; Furneaux, P.A. Mutations in the {beta} subunit of the Bacillus subtilis RNA polymerase that confer both rifampicin resistance and hypersensitivity to NusG. Microbiology 2000, 146, 3041-3049.
53. Maughan, H.; Galeano, B.; Nicholson, W.L. Novel rpoB mutations conferring rifampin resistance on Bacillus subtilis: global effects on growth, competence, sporulation, and germination. J. Bacteriol. 2004, 186, 2481-2486.
54. Ullrich, C.; Kluge, B.; Palacz, Z.; Vater, J. Cell-free biosynthesis of surfactin, a cyclic lipopeptide produced by Bacillus subtilis. Biochemistry 1991, 30, 6503-6508.
55. Youssef, N.H.; Duncan, K.E.; Nagle, D.P.; Savage, K.N.; Knapp, R.M.; McInerney, M.J. Comparison of methods to detect biosurfactant production by diverse microorganisms. J. Microbiol. Meth. 2004, 56, 339-347.
56. Ho, S.N.; Hunt, H.D.; Horton, R.M.; Pullen, J.K.; Pease, L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989, 77, 51-59.
57. Horton, R.M.; Hunt, H.D.; Ho, S.N.; Pullen, J.K.; Pease, L.R. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 1989, 77, 61-68.
58. Yon, J.; Fried, M. Precise gene fusion by PCR. Nucl. Acids Res. 1989, 17, 4895.
59. Cutting, S.M.; Vander Horn, P.B. Genetic analysis. In Molecular Biological Methods for Bacillus; Harwood, C.R., Cutting, S.M., Eds.; John Wiley & Sons Ltd.: Chichester, UK, 1990; Chapter 2, pp. 27-74.
60. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
61. Milne, K.G.; Mehlert, A.; Ferguson, M.A.J. The use of Pseudomonas acyl-CoA synthetase to form acyl-CoAs from dicarboxylic fatty acids. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2001, 1531, 1-3.
62. Alber, B.E.; Fuchs, G. Propionyl-coenzyme A synthase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO2 fixation. J. Biol. Chem. 2002, 277, 12137-12143.
63. Beuerle, T.; Pichersky, E. Enzymatic synthesis and purification of aromatic coenzyme A esters. Anal. Biochem. 2002, 302, 305-312.