Crystal Structure of Long-Chain Alkane Monooxygenase (LadA) in Complex with Coenzyme FMN: Unveiling the Long-Chain Alkane Hydroxylase

Journal of Molecular Biology

Volumn 376, Issue 2, 2008, Pages 453-465

  Li, Liu ^a,b   Liu, Xueqian ^b,c   Yang, Wen ^a   Xu, Feng ^a   Wang, Wei ^a   Feng, Lu ^b,c   Bartlam, Mark ^a,b   Wang, Lei ^b,c   Rao, Zihe ^a,b  

^a TSINGHUA UNIVERSITY   (China)

^b NANKAI UNIVERSITY   (China)

^c Tianjin Research Center for Functional Genomics and Biochip   (China)

Author keywords

alkane degradation; crystal structure; hydroxylase; LadA; monooxygenase

Indexed keywords

ALKANE; FLAVINE MONONUCLEOTIDE; FLAVOPROTEIN; OIL; OXYGENASE; PETROLEUM; PROTEIN LADA; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BIOTECHNOLOGY; CATALYSIS; COENZYME; CRYSTAL STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; POLLUTANT; PRIORITY JOURNAL; PROTEIN DEGRADATION;

BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); GEOBACILLUS THERMODENITRIFICANS;

EID: 38349124762     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.11.069     Document Type: Article

References (50)

1. Feng L., Wang W., Cheng J., Ren Y., Zhao G., Gao C., et al. Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proc. Natl Acad. Sci. USA 104 (2007) 5602-5607
2. Söhngen N.L. Ueber Bakterien, welche Methan als Kohlenstoffnahrung und Energiequelle gebrauchen. Zentralbl. Bakteriol., Parasintenkd., Infektionskrankh. Hyg., Abt. 2 15 (1906) 513-517
3. Söhngen N.L. Benzin, Petroleum, Paraffinöl und Paraffin als Kohlenstoff und Energiequelle für Mikroben. Zentralbl. Bakteriol., Parasintenkd., Infektionskrankh. Hyg., Abt. 2 37 (1913) 595-609
4. van Beilen J.B., Panke S., Lucchini S., Franchini A.G., Rothlisberger M., and Witholt B. Analysis of Pseudomonas putida alkane-degradation gene clusters and flanking insertion sequences: evolution and regulation of the alk genes. Microbiology 147 (2001) 1621-1630
5. Tani A., Ishige T., Sakai Y., and Kato N. Gene structures and regulation of the alkane hydroxylase complex in Acinetobacter sp. strain M-1. J. Bacteriol. 183 (2001) 1819-1823
6. van Beilen J.B., Smits T.H., Whyte L.G., Schorcht S., Rothlisberger M., Plaggemeier T., et al. Alkane hydroxylase homologues in Gram-positive strains. Environ. Microbiol. 4 (2002) 676-682
7. Whyte L.G., Smits T.H., Labbe D., Witholt B., Greer C.W., and van Beilen J.B. Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus strains Q15 and NRRL B-16531. Appl. Environ. Microbiol. 68 (2002) 5933-5942
8. Yadav J.S., and Loper J.C. Multiple p450alk (cytochrome P450 alkane hydroxylase) genes from the halotolerant yeast Debaryomyces hansenii. Gene 226 (1999) 139-146
9. Murrell J.C., Gilbert B., and McDonald I.R. Molecular biology and regulation of methane monooxygenase. Arch. Microbiol. 173 (2000) 325-332
10. Halsey K.H., Sayavedra-Soto L.A., Bottomley P.J., and Arp D.J. Site-directed amino acid substitutions in the hydroxylase alpha subunit of butane monooxygenase from Pseudomonas butanovora: implications for substrates knocking at the gate. J. Bacteriol. 188 (2006) 4962-4969
11. Kotani T., Yamamoto T., Yurimoto H., Sakai Y., and Kato N. Propane monooxygenase and NAD+-dependent secondary alcohol dehydrogenase in propane metabolism by Gordonia sp. strain TY-5. J. Bacteriol. 185 (2003) 7120-7128
12. van Beilen J.B., Wubbolts M.G., and Witholt B. Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5 (1994) 161-174
13. van Beilen J.B., Li Z., Duetz W.A., Smits T.H.M., and Witholt B. Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci. Technol. 58 (2003) 427-440
14. Bernhardt R. Cytochromes P450 as versatile biocatalysts. J. Biotechnol. 124 (2006) 128-145
15. van Beilen J.B., and Funhoff E.G. Alkane hydroxylases involved in microbial alkane degradation. Appl. Microbiol. Biotechnol. 74 (2007) 13-21
16. Ghisla S., and Massey V. Mechanisms of flavoprotein-catalyzed reactions. Eur. J. Biochem. 181 (1989) 1-17
17. Palfey B.A., Ballou D.P., and Massey V. Oxygen activation by flavins and pterins. Active Oxygen: Reactive Oxygen Species in Biochemistry (1995), Chapman & Hall, London, United Kingdom 37-83
18. Palfey B.A., and Massey V. Flavin-dependent enzymes. In: Sinnott M. (Ed). Comprehensive Biological Catalysis, Volume III. Radical Reactions and Oxidation/Reduction (1998), Academic Press, London, United Kingdom 83-154
19. Eichhorn E., van der Ploeg J.R., and Leisinger T. Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli. J. Biol. Chem. 274 (1999) 26639-26646
20. Eichhorn E., Davey C.A., Sargent D.F., Leisinger T., and Richmond T.J. Crystal structure of Escherichia coli alkanesulfonate monooxygenase SsuD. J. Mol. Biol. 324 (2002) 457-468
21. Fisher A.J., Thompson T.B., Thoden J.B., Baldwin T.O., and Rayment I. The 1.5-Å resolution crystal structure of bacterial luciferase in low salt conditions. J. Biol. Chem. 271 (1996) 21956-21968
22. Shima S., Warkentin E., Grabarse W., Sordel M., Wicke M., Thauer R.K., and Ermler U. Structure of coenzyme F(420) dependent methylenetetrahydromethanopterin reductase from two methanogenic archaea. J. Mol. Biol. 300 (2000) 935-950
23. Aufhammer S.W., Warkentin E., Berk H., Shima S., Thauer R.K., and Ermler U. Coenzyme binding in F420-dependent secondary alcohol dehydrogenase, a member of the bacterial luciferase family. Structure 12 (2004) 361-370
24. CCP4. The CCP4 suite-programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763
25. Brünger A.T., Adams P.D., Clore G.M., Delano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system (CNS): a software system for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (1998) 905-921
26. Jones T.A., Zou J.Y., Cowan S., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., Sect. A: Found. Crystallogr. 47 (1991) 110-119
27. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
28. Banner D.W., Bloomer A.C., Petsko G.A., Phillips D.C., Pogson C.I., and Wilson I.A. Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 Å resolution. Nature 255 (1975) 609-614
29. Thompson J.D., Higgins D.G., and Gibson T.J. 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 (1994) 4673-4680
30. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-138
31. 420/FMN binding site of enzymes within the nonprolyl cis-peptide containing bacterial luciferase family. Protein Sci. 14 (2005) 1840-1849
32. Lindqvist Y. Refined structure of spinach glycolate oxidase at 2 Å resolution. J. Mol. Biol. 209 (1989) 151-166
33. Xia Z.X., and Mathews F.S. Molecular structure of flavocytochrome b2 at 2.4 Å resolution. J. Mol. Biol. 212 (1990) 837-863
34. Lim L.W. Three-dimensional structure of the iron-sulfur flavoprotein trimethylamine dehydrogenase at 2.4 Å resolution. J. Biol. Chem. 261 (1986) 15140-15146
35. Fox K.M., and Karplus P.A. Old yellow enzyme at 2 Å resolution: overall structure, ligand binding, and comparison with related flavoproteins. Structure 2 (1994) 1089-1105
36. Rowland P., Nielsen F.S., Jensen K.F., and Larsen S. The crystal structure of the flavin containing enzyme dihydroorotate dehydrogenase A from Lactococcus lactis. Structure 5 (1997) 239-252
37. Farber G.K., and Petsko G.A. The evolution of alpha/beta barrel enzymes. Trends Biochem. Sci. 15 (1990) 228-234
38. Alfieri A., Fersini F., Ruangchan N., Prongjit M., Chaiyen P., and Mattevi A. Structure of the monooxygenase component of a two-component flavoprotein monooxygenase. Proc. Natl Acad. Sci. USA 104 (2007) 1177-1182
39. Schreuder H.A., Prick P.A.J., Wierenga R.K., Vriend G., Wilson K.S., Hol W.G.J., and Drenth J. Crystal structure of the p-hydroxybenzoate hydroxylase-substrate complex refined at 1.9 Å resolution. Analysis of the enzyme-substrate and enzyme-product complexes. J. Mol. Biol. 208 (1989) 679-696
40. Gatti D.L., Palfey B.A., Lah M.S., Entsch B., Massey V., Ballou D.P., and Ludwig M.L. The mobile flavin of 4-OH benzoate hydroxylase. Science 266 (1994) 110-114
41. Hiromoto T., Fujiwara S., Hosokawa K., and Yamaguchi H. Crystal structure of 3-hydroxybenzoate hydroxylase from Comamonas testosteroni has a large tunnel for substrate and oxygen access to the active site. J. Mol. Biol. 364 (2006) 878-896
42. Dong C., Flecks S., Unversucht S., Haupt C., van Pee K.H., and Naismith J.H. Tryptophan 7-halogenase (PrnA) structure suggests a mechanism for regioselective chlorination. Science 309 (2005) 2216-2219
43. Malito E., Alfieri A., Fraaije M.W., and Mattevi A. Crystal structure of a Baeyer-Villiger monooxygenase. Proc. Natl Acad. Sci. USA 101 (2004) 13157-13162
44. Jeffers C.E., Nichols J.C., and Tu S.C. Complex formation between Vibrio harveyi luciferase and monomeric NADPH:FMN oxidoreductase. Biochemistry 42 (2003) 529-534
45. Maeng J.H., Sakai Y., Tani Y., and Kato N. Isolation and characterization of a novel oxygenase that catalyzes the first step of n-alkane oxidation in Acinetobacter sp. strain M-1. J. Bacteriol. 178 (1996) 3695-3700
46. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
47. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 2126-2132
48. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 (1997) 240-255
49. Morris G.M., Goodsell D.S., Halliday R.S., Huey R., Hart W.E., Belew R.K., and Olson A.J. Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J. Comput. Chem. 9 (1998) 1662-1939
50. Wang L., Tang Y., Wang S., Liu R.L., Liu M.Z., Zhang Y., et al. Isolation and characterization of a novel thermophilic Bacillus strain degrading long-chain n-alkanes. Extremophiles 10 (2006) 347-356