Investigation of cytochromes P450 in myxobacteria: Excavation of cytochromes P450 from the genome of Sorangium cellulosum so ce56

FEBS Letters

Volumn 585, Issue 11, 2011, Pages 1506-1513

  Khatri, Yogan ^a   Hannemann, Frank ^a   Perlova, Olena ^a   Müller, Rolf ^a   Bernhardt, Rita ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

CYPome; Cytochrome P450; Haliangium ochraceum; Myxococcus xanthus; Sorangium cellulosum So ce56; Stigmatella aurantiaca

Indexed keywords

BACTERIAL ENZYME; CYP109D1; CYP110H1; CYP110J1; CYP124E1; CYP260A1; CYP261A1; CYP262A1; CYP262B1; CYP263A1; CYP264A1; CYP264B1; CYP266A1; CYP267B1; CYTOCHROME P450; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE SEQUENCE; GENETIC ORGANIZATION; HALIANGIUM OCHRACEUM; MICROBIAL DIVERSITY; MYXOCOCCALES; MYXOCOCCUS XANTHUS; NONHUMAN; NUCLEOTIDE SEQUENCE; P450 GENE; PHYLOGENETIC TREE; PRIORITY JOURNAL; REVIEW; SORANGIUM CELLULOSUM; SPECIES COMPARISON; SPOROGENESIS; STIGMATELLA AURANTIACA;

CYTOCHROME P-450 ENZYME SYSTEM; GENOME, BACTERIAL; GENOMICS; MYXOCOCCALES; SPORES, BACTERIAL;

HALIANGIUM OCHRACEUM; MYXOCOCCALES; MYXOCOCCUS XANTHUS; POLYANGIUM CELLULOSUM; STIGMATELLA AURANTIACA;

EID: 79957576732     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.04.035     Document Type: Review

References (72)

1. R. Bernhardt Cytochrome P450: structure, function and generation of reactive oxygen species Rev. Physiol. Biochem. Pharmacol. 127 1996 1 80
2. R. Bernhardt Cytochromes P450 as versatile biocatalysts J. Biotechnol. 124 2006 128 145 (Pubitemid 43816140)
3. R. Bernhardt, and M.R. Waterman The ubiquitous roles of cytochrome P450 proteins A. Sigel, H. Sigel, R.K.O. Sigel, 2007 John Wiley & Sons pp. 361-396
4. B. Zhao, X. Lin, L. Lei, D.C. Lamb, S.L. Kelly, M.R. Waterman, and D.E. Cane Biosynthesis of the sesquiterpene antibiotic albaflavenone in Streptomyces coelicolor A3(2) J. Biol. Chem. 283 2008 8183 8189
5. K. Buntin, S. Rachid, M. Scharfe, H. Blöcker, J.K. Weissman, and R. Müller Production of the antifungal isochromanone a judazols A and B in Chondromyces crocatus Cm c5: biosynthetic machinery and cytochrome P450 modifications Angew. Chem. Int. Ed. Engl. 47 2008 4595 4599
6. S. Malla, T.T. Thuy, T.J. Oh, and J.K. Sohng Identification and characterization of gerPI and gerPII involved in epoxidation and hydroxylation of dihydrochalcolactone in Streptomyces species KCTC 0041BP Arch. Microbiol. 193 2011 95 103
7. F. Hannemann, A. Bichet, K.M. Ewen, and R. Bernhardt Cytochrome P450 systems-biological variations of electron transport chains Biochem. Biophys. Acta. Gen. Sub. 1770 2007 330 344 (Pubitemid 46157074)
8. D. Kaiser Coupling cell movement to multicellular development in myxobacteria Nat. Rev. Micro. 1 2003 45 54
9. L.J. Shimkets, M. Dworkin, and H. Reichenbach The Myxobacteria 2005 Springer-Verlag New York, NY
10. H. Reichenbach, and M. Dworkin The order Myxobacterales M.P. Starr, H.G. Trüper, A. Balows, H.G. Schlegel, The Prokaryotes 1992 Springer-Verlag Berlin pp. 328-355
11. T.F. Schäberle, E. Goralski, E. Neu, O. Erol, G. Hölzl, P. Dörmann, G. Bierbaum, and G.M. König Marine myxobacteria as a source of antibiotics-comparison of physiology, polyketide-type genes and antibiotic production of three new isolates of Enhygromyxa salina Mar. Drugs. 8 2010 2466 2479
12. R.O. Garcia, D. Krug, and R. Müller Discovering natural products from myxobacteria with emphasis on rare producer strains in combination with improved analytical methods Methods Enzymol. 458 2009 59 91
13. K.J. Weissman, and R. Müller Myxobacterial secondary metabolites bioactivities and modes-of-action Nat Prod Rep. 2010 September 18 27 9 2010 1276 1295
14. K. Gerth, S. Pradella, O. Perlova, S. Beyer, and R. Müller Myxobacteria: proficient producers of novel natural products with various biological activities-past and future biotechnological aspects with the focus on the genus Sorangium J. Biotechnol. 106 2003 233 253 (Pubitemid 37494861)
15. Kopp, M., Irschik, H., Gemperlein, K., Buntin, K., Meiser, P., Weissman, K.J., Bode, H.B., and Müller R. (2011). Insights into the complex biosynthesis of the leupyrrins in Sorangium cellulosum So ce690. Mol. Biosyst. doi: 10.1039/C0MB00240B.
16. H. Irschik, H. Reichenbach, G. Höfle, and R. Jansen The thuggacins, novel antibacterial macrolides from Sorangium cellulosum acting against selected Gram-positive bacteria J. Antibiot. 60 2007 733 738
17. H. Irschik, M. Kopp, K.J. Weissman, K. Buntin, J. Piel, and R. Müller Analysis of the sorangicin gene cluster reinforces the utility of a combined phylogenetic/retrobiosynthetic analysis for deciphering natural product assembly by trans-AT PKS Chem. Bio. chem. 11 2010 1840 1849
18. W.J. Guo, and W.Y. Tao Phoxalone, a novel macrolide from Sorangium cellulosum: structure identification and its anti-tumor bioactivity in vitro Biotechnol. Lett. 30 2008 349 356
19. J.W. Ahn, K.H. Jang, S.C. Chung, K.B. Oh, and J. Shin Sorangiadenosine, a new sesquiterpene adenoside from the myxobacterium Sorangium cellulosum Org. Lett. 10 2008 1167
20. X. Li, T.K. Yu, J.H. Kwak, B.Y. Son, Y. Seo, O.P. Zee, and J.W. Ahn Soraphinol C, a new free-radical scavenger from Sorangium cellulosum J. Microbiol. Biotechnol. 18 2008 520 522
21. H.J. Mulzer The Epothilones - An Outstanding Family of Anti-Tumor Agents: From Soil to the Clinic 2008 Springer-Verlag Austria
22. S. Schneiker, O. Perlova, O. Kaiser, K. Gerth, A. Alici, M.O. Altmeyer, D. Bartels, T. Bekel, S. Beyer, E. Bode, H.B. Bode, C.J. Bolten, J.V. Choudhuri, S. Doss, Y.A. Elnakady, B. Frank, L. Gaigalat, A. Goesmann, C. Groeger, F. Gross, L. Jelsbak, L. Jelsbak, J. Kalinowski, C. Kegler, T. Knauber, S. Konietzny, M. Kopp, L. Krause, D. Krug, B. Linke, T. Mahmud, R. Martinez-Arias, A.C. McHardy, M. Merai, F. Meyer, S. Mormann, J. Munoz-Dorado, J. Perez, S. Pradella, S. Rachid, G. Raddatz, F. Rosenau, C. Ruckert, F. Sasse, M. Scharfe, S.C. Schuster, G. Suen, A. Treuner-Lange, G.J. Velicer, F.-J. Vorholter, K.J. Weissman, R.D. Welch, S.C. Wenzel, D.E. Whitworth, S. Wilhelm, C. Wittmann, H. Blocker, A. Puhler, and R. Müller Complete genome sequence of the myxobacterium Sorangium cellulosum Nat. Biotech. 25 2007 1281 1289 (Pubitemid 350076516)
23. C.S. Wenzel, and R. Müller Myxobacterial natural product assembly lines: fascinating examples of curious biochemistry Nat. Prod. Rep. 24 2007 1211 1224 (Pubitemid 350151358)
24. D. Menche, F. Arikan, O. Perlova, N. Horstmann, W. Ahlbrecht, S.C. Wenzel, R. Jansen, H. Irschik, and R. Müller Stereochemical determination and complex biosynthetic assembly of ethangien, a highly potent RNA-polymerase inhibitor from the myxobacterium Sorangium cellulosum J. Am. Chem. Soc. 130 2008 14234 14243
25. J. Perez, A. Castaneda-Garcia, H. Jenke-Kodama, R. Müllar, and J. Munoz-Dorado Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome Proc. Natl. Acad. Sci. USA 105 2008 15950 15955
26. D.R. Nelson Progress in tracing the evolutionary paths of cytochrome P450 Biochim. Biophys. Acta. 1814 2011 14 18
27. Y. Khatri, F. Hannemann, K.M. Ewen, D. Pistorius, O. Perlova, N. Kagawa, A.O. Brachmann, R. Müller, and R. Bernhardt The CYPome of Sorangium cellulosum So ce56 and identification of CYP109D1 as a new fatty acid hydroxylase Chem. Biol. 17 2010 1295 1305
28. B. Goldman, S. Bhat, and L.J. Shimkets Genome evolution and the emergence of fruiting body development in Myxococcus xanthus PLoS One 2 2007 e1329
29. S. Huntley, N. Hamann, S. Wegener-Feldbrügge, A. Treuner-Lange, M. Kube, R. Reinhardt, S. Klages, R. Müller, C.M. Ronning, W.C. Nierman, and L. Søgaard-Andersen Comparative genomic analysis of fruiting body formation in myxococcales Mol. Biol. Evol. 28 2011 1083 1097
30. N. Ivanova, C. Daum, E. Lang, B. Abt, M. Kopitz, E. Saunders, A. Lapidus, S. Lucas, T. Glavina Del Rio, M. Nolan, H. Tice, A. Copeland, J.F. Cheng, F. Chen, D. Bruce, L. Goodwin, S. Pitluck, K. Mavromatis, A. Pati, N. Mikhailova, A. Chen, K. Palaniappan, M. Land, L. Hauser, Y.J. Chang, C.D. Jeffries, J.C. Detter, T. Brettin, M. Rohde, M. Goker, J. Bristow, V. Markowitz, J.A. Eisen, P. Hugenholtz, N.C. Kyrpides, and H.P. Klenk Complete genome sequence of Haliangium ochraceum type strain (SMP-2) Stand. Genomic. Sci. 2 2010 96 106
31. S.H. Thomas, R.D. Wagner, A.K. Arakaki, J. Skolnick, J.R. Kirby, L.J. Shimkets, R.A. Sanford, and F.E. Loffler The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta-proteobacteria PLoS One 3 2008 e2103
32. R.A. Sanford, J.R. Cole, and J.M. Tiedje Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp.nov., an aryl-halorespiring facultative anaerobic Myxobacterium Appl. Environ. Microbiol. 68 2002 893 900 (Pubitemid 34113082)
33. K.M. Ewen, F. Hannemann, Y. Khatri, O. Perlova, R. Kappl, D. Krug, J. Hüttermann, R. Müller, and R. Bernhardt Genome mining in Sorangium Cellulosum So ce56-Identification and characterization of the homologous electron transfer proteins of a myxobacterial cytochrome P450 J. Biol. Chem. 284 2009 28590 28598
34. B. Frank, S.C. Wenzel, H.B. Bode, M. Scharfe, H. Blocker, and R. Müller Genetic diversity to metabolic unity: studies on the biosynthesis of aurafurones and aurafuron-like structures in myxobacteria and streptomycetes J. Mol. Biol. 374 2007 24 38 (Pubitemid 47600238)
35. Y. Khatri, M. Girhard, A. Romankiewicz, M. Ringle, F. Hannemann, V.B. Urlacher, M.C. Hutter, and R. Bernhardt Regioselective hydroxylation of norisoprenoids by CYP109D1 from Sorangium cellulosum So ce56 Appl. Microbiol. Biotechnol. 88 2010 485 495
36. K.J. McLean, D. Clift, D.G. Lewis, M. Sabri, P.R. Balding, M.J. Sutcliffe, D. Leys, and A.W. Munro The preponderance of P450s in the Mycobacterium tuberculosis genome Trends Microbiol. 14 2006 5
37. D.C. Lamb, T. Skaug, H.L. Song, C.J. Jackson, L.M. Podust, M.R. Waterman, D.B. Kell, D.E. Kelly, and S.L. Kelly The cytochrome P450 complement (CYPome) of Streptomyces coelicolor A3(2) J. Biol. Chem. 277 2002 24000 24005 (Pubitemid 34951911)
38. D.B. Hawkes, G.W. Adams, A.L. Burlingame, P.R. Ortiz de Montellano, and J.J. De Voss Cytochrome P450(cin) (CYP176A), isolation, expression, and characterization J. Biol. Chem. 277 2002 27725 27732 (Pubitemid 34966716)
39. M.J. Cryle, N.J. Matovic, and J.J. De Voss Products of cytochrome P450(BioI) (CYP107H1)-catalyzed oxidation of fatty acids Org. Lett. 5 2003 3341 3344 (Pubitemid 37140708)
40. B. Simgen, J. Contzen, R. Schwarzer, R. Bernhardt, and C. Jung Substrate binding to 15beta-hydroxylase (CYP106A2) probed by FT infrared spectroscopic studies of the iron ligand CO stretch vibration Biochem. Biophys. Res. Commun. 269 2000 737 742 (Pubitemid 30440371)
41. M.A. McLean, S.A. Maves, K.E. Weiss, S. Krepich, and S.G. Sligar Characterization of a cytochrome P450 from the acidothermophilic archaea Sulfolobus solfataricus Biochem. Biophys. Res. Commun. 252 1998 166 172 (Pubitemid 28534645)
42. A. Shafiee, and C.R. Hutchinson Macrolide antibiotic biosynthesis: isolation and properties of two forms of 6-deoxyerythronolide B hydroxylase from Saccharopolyspora erythraea (Streptomyces erythreus) Biochemistry 26 1987 6204 6210 (Pubitemid 17153324)
43. M. Haniu, L.G. Armes, M. Tanaka, K.T. Yasunobu, B.S. Shastry, G.C. Wagner, and I.C. Gunsalus The primary structure of the monoxygenase cytochrome P450cam Biochem. Biophys. Res. Commun. 105 1982 889 894
44. C.A. Morgan, and R.C. Wyndham Characterization of TDT genes for the degradation of tricyclic diterpenes by Pseudomonas diterpeniphila A19-6a Can. J. Microbiol. 48 2002 49 59 (Pubitemid 34258650)
45. B. Julien, S. Shah, R. Ziermann, R. Goldman, L. Katz, and C. Khosla Isolation and characterization of the epothilone biosynthetic gene cluster from Sorangium cellulosum Gene 249 2000 153 160 (Pubitemid 30265497)
46. M.K. Trower, F.S. Sariaslani, and D.P. O'Keefe Purification and characterization of a soybean flour-induced cytochrome P-450 from Streptomyces griseus J. Bacteriol. 171 1989 1781 1787 (Pubitemid 19103938)
47. A. Celik, S.L. Flitsch, and N.J. Turner Efficient terpene hydroxylation catalysts based upon P450 enzymes derived from actinomycetes Org. Biomol. Chem. 3 2005 2930 2934 (Pubitemid 41239069)
48. B. Frank, J. Knauber, H. Steinmetz, M. Scharfe, H. Blöcker, S. Beyer, and R. Müller Spiroketal polyketide formation in Sorangium: identification and analysis of the biosynthetic gene cluster for the highly cytotoxic spirangienes Chem. Biol. 14 2007 221 233 (Pubitemid 46274422)
49. H.B. Bode, H. Irschik, S.C. Wenzel, H. Reichenbach, R. Müller, and G. Höfle The leupyrrins: a structurally unique family of secondary metabolites from the myxobacterium Sorangium cellulosum J. Nat. Prod. 66 2003 1203 1206 (Pubitemid 37204219)
50. A. Green, S. Rivers, M. Cheesman, G. Reid, L. Quaroni, I. Macdonald, S. Chapman, and A. Munro Expression, purification and characterization of cytochrome P450 BioI: a novel P450 involved in biotin synthesis in Bacillus subtilis J. Biol. Inorg. Chem. 6 2001 523 533 (Pubitemid 32822113)
51. M. Girhard, T. Klaus, Y. Khatri, R. Bernhardt, and V.B. Urlacher Characterization of the versatile monooxygenase CYP109B1 from Bacillus subtilis Appl. Microbiol. Biotechnol. 87 2010 595 607
52. Y.J. Chun, T. Shimada, R. Sanchez-Ponce, M.V. Martin, L. Lei, B. Zhao, S.L. Kelly, M.R. Waterman, D.C. Lamb, and F.P. Guengerich Electron transport pathway for a Streptomyces Cytochrome P450: Cytochrome P450 105D5-catalyzed fatty acid hydroxylation in Streptomyces coelicolor A3(2) J. Biol. Chem. 282 2007 17486 17500 (Pubitemid 47100286)
53. S. Torres, C. Fjetland, and P. Lammers Alkane-induced expression, substrate binding profile, and immunolocalization of a cytochrome P450 encoded on the nifD excision element of Anabaena 7120 BMC Microbiol. 5 2005 16
54. R.E. Tully, P. van Berkum, K.W. Lovins, and D.L. Keister Identification and sequencing of a cytochrome P450 gene cluster from Bradyrhizobium japonicum Biochem. Biophys. Acta 1398 1998 243 255 (Pubitemid 28338161)
55. J.K. Capyk, R. Kalscheuer, G.R. Stewart, J. Liu, H. Kwon, R. Zhao, S. Okamoto, W.R. Jacobs Jr., L.D. Eltis, and W.W. Mohn Mycobacterial cytochrome p450 125 (cyp125) catalyzes the terminal hydroxylation of c27 steroids J. Biol. Chem. 284 2009 35534 35542
56. K.J. McLean, P. Lafite, C. Levy, M.R. Cheesman, N. Mast, I.A. Pikuleva, D. Leys, and A.W. Munro The Structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection J. Biol. Chem. 284 2009 35524 35533
57. C.H. Kosla, and P.B. Harbury Modular enzymes Nature 409 2001 247 252 (Pubitemid 32144294)
58. N. Parajuli, D.B. Basnet, L.H. Chan, J.K. Sohng, and K. Liou Genome analyses of Streptomyces peucetius ATCC 27952 for the identification and comparison of cytochrome P450 complement with other Streptomyces Arch. Biochem. Biophys. 425 2004 233 241 (Pubitemid 38542816)
59. B. Zhao, and M.R. Waterman Novel properties of P450s in Streptomyces coelicolor Drug Metabol. Rev. 39 2007 343 352 (Pubitemid 47355732)
60. H. Chen, and C.T. Walsh Coumarin formation in novobiocin biosynthesis: beta-hydroxylation of the aminoacyl enzyme tyrosyl-S-NovH by a cytochrome P450 NovI Chem. Biol. 8 2001 301 312 (Pubitemid 32442486)
61. M.L. Dickens, N.D. Priestley, and W.R. Strohl In vivo and in vitro bioconversion of epsilon-rhodomycinone glycoside to doxorubicin: functions of DauP, DauK, and DoxA J. Bacteriol. 179 1997 2641 2650 (Pubitemid 27164564)
62. P. Caffrey, S. Lynch, E. Flood, S. Finnan, and M. Oliynyk Amphotericin biosynthesis in Streptomyces nodosus: deductions from analysis of polyketide synthase and late genes Chem. Biol. 8 2001 713 723 1 (Pubitemid 32632537)
63. H.T. Chiu, B.K. Hubbard, A.N. Shah, J. Eide, R.A. Fredenburg, C.T. Walsh, and C. Khosla Molecular cloning and sequence analysis of the complestatin biosynthetic gene cluster Proc. Natl. Acad. Sci. USA 98 2001 8548 8553 (Pubitemid 32678065)
64. H. Ikeda, T. Nonomiya, M. Usami, T. Ohta, and S. Omura Organization of the biosynthetic gene cluster for the polyketide anthelmintic macrolide avermectin in Streptomyces avermitilis Proc. Natl. Acad. Sci. USA 96 1999 9509 9514 (Pubitemid 29398761)
65. M.A. Austin, M. Izumikawa, M.E. Bowman, D.W. Udwary, J.L. Ferrer, B.S. Moore, and J.P. Nol Crystal structure of a bacterial type III polyketide synthase and enzymatic control of reactive polyketide intermediate J. Biol. Chem. 279 2004 45162 45174 (Pubitemid 39430932)
66. R. Quaderer, S. Omura, H. Ikeda, and D.E. Cane Pentalenolactone biosynthesis. Molecular cloning and assignment of biochemical function to PtlI, a cytochrome P450 of Streptomyces avermitilis J. Am. Chem. Soc. 128 2006 13036 13037 (Pubitemid 44527659)
67. L. Jelsbak, M. Givskov, and D. Kaiser Enhancer-binding proteins with a forkhead-associated domain and the {sigma}54 regulon in Myxococcus xanthus fruiting body development Proc. Natl. Acad. Sci. USA 102 2005 3010 3015 (Pubitemid 40299907)
68. J.N. Hamlin, R.A. Bloodworth, and S.T. Cardona Regulation of phenylacetic acid degradation genes of Burkholderia cenocepacia K56-2 BMC Microbiol. 9 2009 222
69. J.M. Luengo, J.L. Garcia, and E.R. Olivera The phenylacetyl-CoA catabolon: a complex catabolic unit with broad biotechnological applications Mol. Microbiol. 39 2001 1434 1442 (Pubitemid 32269741)
70. J.B. Johnston, P.M. Kells, L.M. Podust, and P.R. Ortiz de Montellano Biochemical and structural characterization of CYP124: a methyl-branched lipid omega-hydroxylase from Mycobacterium tuberculosis Proc. Natl. Acad. Sci. USA 106 2009 20687 20692
71. J.B. Johnston, H. Ouellet, and P.R. Ortiz de Montellano Functional redundancy of steroid C26-monooxygenase activity in Mycobacterium tuberculosis revealed by biochemical and genetic analyses J. Biol. Chem. 285 2010 36352 36360
72. M. Girhard, K. Machida, M. Itoh, R.D. Schmid, A. Arisawa, and V.B. Urlacher Regioselective biooxidation of (+)-valencene by recombinant E. coli expressing CYP109B1 from Bacillus subtilis in a two-liquid-phase system. Microb Cell Fact 8 2009 36