CYP116B5: A new class VII catalytically self-sufficient cytochrome P450 from Acinetobacter radioresistens that enables growth on alkanes

Molecular Microbiology

Volumn 95, Issue 3, 2015, Pages 539-554

  Minerdi, Daniela ^a   Sadeghi, Sheila J ^a   Di Nardo, Giovanna ^a   Rua, Francesco ^a   Castrignanò, Silvia ^a   Allegra, Paola ^a   Gilardi, Gianfranco ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALKANE; CYTOCHROME P450; CYTOCHROME P450 116B5; UNCLASSIFIED DRUG; HEME; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RECOMBINANT PROTEIN;

ACINETOBACTER; ACINETOBACTER RADIORESISTENS; ALKB GENE; ALMA GENE; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BINDING SITE; CARBON SOURCE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYP116B5 GENE; ESCHERICHIA COLI; EVOLUTION; GENE EXPRESSION; GENE FUSION; HETEROLOGOUS EXPRESSION; HORIZONTAL GENE TRANSFER; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; RHODOCOCCUS JOSTII; BIOCATALYSIS; CHEMISTRY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; ITALY; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; RHODOCOCCUS; SEQUENCE ALIGNMENT;

ACINETOBACTER RADIORESISTENS; ESCHERICHIA; RHODOCOCCUS;

ACINETOBACTER; ALKANES; AMINO ACID SEQUENCE; BINDING SITES; BIOCATALYSIS; BIOLOGICAL EVOLUTION; CYTOCHROME P-450 ENZYME SYSTEM; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; HEME; ITALY; MOLECULAR SEQUENCE DATA; NADP; OXIDATION-REDUCTION; PHYLOGENY; RECOMBINANT PROTEINS; RHODOCOCCUS; SEQUENCE ALIGNMENT; SOIL MICROBIOLOGY;

EID: 84924565455     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12883     Document Type: Article

References (46)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Barbe, V., Vallenet, D., Fonknechten, N., Kreimeyer, A., Oztas, S., Labarre, L., Cruveiller, C., Robert, C., etal. (2004) Unique features revealed by the genome sequence of Acinetobacter sp. ADP1, a versatile and naturally transformation competent bacterium. Nucleic Acids Res 32: 5766-5779.
3. van Beilen, J.B., and Funhoff, E.G. (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74: 13-21.
4. van Beilen, J.B., Marin, M.M., Smits, T.H., Rothlisberger, M.A.G., Witholt, B., and Rojo, F. (2004) Characterization of two alkane hydroxylase genes from the marine hydrocarbonoclastic bacterium Alcanivorax borkumensis. Environ Microbiol 6: 264-273.
5. van Berkel, W.J.H., Kamerbeek, N.M., and Fraaije, M.W. (2006) Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts. J Biotechnol 124: 670-676.
6. Bernhardt, R. (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124: 128-145.
7. Bühler, M., and Schindler, J. (1984) Aliphatic hydrocarbons. In Biotransformations. Kieslich, K. (ed.). Verlag Chemie Weinheim, Weinheim, Germany. pp. 329-385.
8. Cardini, G., and Jurtshuk, P. (1970) The enzymatic hydroxylation of n-octane by Corynebacterium sp. strain 7E1C. J Biol Chem 245: 2789-2796.
9. Chen, M.M.Y., Snow, C.D., Vizcarra, C.L., Mayo, S.L., and Arnold, F.H. (2012) Comparison of random mutagenesis and semi-rational designed libraries for improved cytochrome P450 BM3-catalyzed hydroxylation of small alkanes. Protein Eng Des Sel 25: 171-178.
10. Correll, D.L., Jordan, T.E., and Weller, D.E. (1992) Nutrient flux in a landscape: effects of coastal land use and terrestrial community mosaic on nutrient transport to coastal waters. Estuaries 15: 431-442.
11. De Mot, R., and Parret, A.H. (2002) A novel class of self-sufficient cytochrome P450 monooxygenases in prokaryotes. Trends Microbiol 10: 502-508.
12. Dodhia, V.R., and Gilardi, G. (2009) Cytochromes P450: tailoring a class of enzymes for biosensing. In Engineering the Bioelectronic Interface. Davis, J. (ed.). London, UK: RSC Publishing, pp. 154-193.
13. Eggink, G., van Lelyveldg, P.H., Arnberg, A., Arfman, N., Witteveen, C., and Witholt, B. (1987) Structure of the Pseudomonas putida alkBAC operon. Identification of transcription and translation products. J Biol Chem 262: 6400-6406.
14. Gassner, G.T., Ludwig, M.L., Gatti, D.L., Correll, C.C., and Ballou, D.P. (1995) Structure and mechanism of the iron-sulfur flavoprotein phthalate dioxygenase reductase. FASEB J 9: 1411-1418.
15. Gustafsson, M.C.U. (2000) Bacterial cytochromes P450: studies on cytochrome P450 102A2 and P450 102A3 of Bacillus subtilis. PhD thesis, Lund University, Lund, Sweden.
16. Hakemian, A.S., and Rosenzweig, A.C. (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76: 223-241.
17. Hannemann, F., Bichet, A., Ewen, K.M., and Bernhardt, R. (2007) Cytochrome P450 systems-biological variations of electron transport chains. Biochim Biophys Acta 1770: 330-344.
18. Hunter, D.J., Roberts, G.A., Ost, T.W., White, J.H., Muller, S., Turner, N.J., Flitsch, S.L., and Chapman, S.K. (2005) Analysis of the domain properties of the novel cytochrome P450 RhF. FEBS Lett 579: 2215-2220.
19. Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120.
20. Kitazume, T., Takaya, N., Nakayama, N., and Shoun, H. (2000) Fusarium oxysporum fatty-acid subterminal hydroxylase (CYP505) is a membrane-bound eukaryotic counterpart of Bacillus megaterium cytochrome P450-BM3. J Biol Chem 275: 39734-39740.
21. Koch, D.J., Chen, M.M., van Beilen, J.B., and Arnold, F.H. (2009) In vivo evolution of butane oxidation by terminal alkane hydroxylases AlkB and CYP153A6. Appl Environ Microbiol 75: 337-344.
22. Koonin, E.V., Makarova, K.S., and Aravind, L. (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Ann Rev Microbiol 55: 709-742.
23. Leak, D.J., Sheldon, R.A., Woodley, J.M., and Adlercreutz, P. (2009) Biocatalysts for selective introduction of oxygen. Biocatal Biotransformation 27: 1-26.
24. Lieberman, R.L., and Rosenzweig, A.C. (2004) Biological methane oxidation: regulation, biochemistry, and active site structure of particulate methane monooxygenase. Crit Rev Biochem Mol Biol 39: 147-164.
25. Maier, T., Foerster, H.H., Asperger, O., and Hahn, U. (2001) Molecular Characterization of the 56-kDa CYP153 from Acinetobacter sp. EB104. Biochem Biophys Res Commun 286: 652-658.
26. Marcotte, E., Pellegrini, M., Yeates, T., and Eisenberg, D. (1999) A census of protein repeats. J Mol Biol 293: 151-160.
27. Minerdi, D., Zgrablic, I., Sadeghi, S.J., and Gilardi, G. (2012) Identification of a novel Baeyer-Villiger monooxygenase from Acinetobacter radioresistens: close relationship to the Mycobacterium tuberculosis prodrug activator EtaA. Microb Biotechnol 5: 700-716.
28. Muller, R., Asperger, O., and Kleber, H.P. (1989) Purification of Cytochrome P-450 from n-hexadecane-grown Acinetobacter Calcoaceticus. Biome Bioche Act 48: 243-254.
29. Narhi, L.O., and Fulco, A.J. (1986) Characterization of a catalytically self-sufficient 119, 000 dalton cytochrome P450 monooxygenase induced by barbiturates in Bacillus megaterium. J Biol Chem 261: 7160-7169.
30. Notomista, E., Lahm, A., Di Donato, A., and Tramontano, A. (2003) Evolution of bacterial and archaeal multicomponent monooxygenases. J Mol Evol 56: 435-445.
31. Pessione, E., and Giunta, C. (1997) Acinetobacter radioresistens metabolizing aromatic compounds. Biochemical and microbiological characterization of the strain. Microbios 89: 105-117.
32. Roberts, G.A., Grogan, G., Greter, A., Flitsch, S.L., and Turner, N.J. (2002) Identification of a new class of cytochrome P450 from a Rhodococcus sp. J Bacteriol 184: 3898-3908.
33. Roberts, G.A., Celik, A., Hunter, D.J., Ost, T.W., White, J.H., Chapman, S.K., Turner, N.J., and Flitsch, S.C. (2003) A self-sufficient cytochrome P450 with a primary structural organization that includes a flavin domain and a [2Fe-2S] redox center. J Biol Chem 278: 48914-48920.
34. Sadeghi, S.J., and Gilardi, G. (2013) Chimeric P450 Enzymes: activity of artificial redox fusions driven by different reductases for biotechnological applications. Biotechnol Appl Biochem 60: 102-110.
35. Saitou, N., and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
36. Sakai, Y., Maeng, J.H., Tani, Y., and Kato, N. (1994) Use oflong-chain n-alkanes (C13-C44) by an isolate, Acinetobacter sp. M-1. Biosci Biotechnol Biochem 58: 2128-2130.
37. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
38. Schneiker, S., Martins dos Santos, V.A., Bartels, D., Bekel, T., Brecht, M., Buhrmester, J., Chemikova, T.N., Denaro, R., etal. (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24: 997-1004.
39. Smits, T.H., Balada, S.B., Witholt, B., and Van Beilen, J.B. (2002) Functional analysis of alkane hydroxylases from Gram-negative and Gram-positive bacteria. J Bacteriol 184: 1733-1742.
40. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
41. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTALW: 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.
42. Throne-Holst, M., Markussen, S., Winnbergm, A., Ellingsen, T.E., Kotlar, H.K., and Zotchev, S.B. (2006) Utilization of n-alkanes by a newly isolated strain of Acinetobacter venetianus: the role of two AlkB-type alkane hydroxylases. Appl Microbiol Biotechnol 72: 353-360.
43. Towner, K.J. (2009) Acinetobacter: an old friend, but a new enemy. J Hosp Infect 73: 355-363.
44. Whyte, L.G., Smits, T.H.M., Labbe, D., Witholt, B., Greer, C.W., and Van Beilen, J.B. (2002) Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus strains Q15 and NRRL B-16531. Appl Environ Microbiol 68: 5933-5942.
45. Wood, T.K. (2008) Molecular approaches in bioremediation. Curr Opin Biotechnol 19: 57.
46. Yanai, I., Derti, A., and DeLisi, C. (2001) Genes linked by fusion events are generally of the same functional category: a systematic analysis of 30 microbial genomes. Proc Natl Acad Sci U S A 98: 7940-7945.