Structural Characterization of Pandoraea pnomenusa B-356 Biphenyl Dioxygenase Reveals Features of Potent Polychlorinated Biphenyl-Degrading Enzymes

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Colbert, Christopher L ^a,g   Agar, Nathalie Y R ^b,e   Kumar, Pravindra ^c,g   Chakko, Mathew N ^d,g   Sinha, Sangita C ^a   Powlowski, Justin B ^e   Eltis, Lindsay D ^f   Bolin, Jeffrey T ^g  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY ROORKEE   (India)

^d PROVIDENCE HOSPITAL   (United States)

^e Gina Cody School of Engineering and Computer Science   (Canada)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^g PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIPHENYL; BIPHENYL DIOXYGENASE; DICHLOROBIPHENYL; DIOXYGENASE; FERROUS ION; POLYCHLORINATED BIPHENYL; UNCLASSIFIED DRUG; WATER;

ARTICLE; BACTERIUM; BETA CHAIN; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PANDORAEA PNOMENUSA; PHYLOGENY; STEADY STATE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

BIPHENYL COMPOUNDS; BURKHOLDERIACEAE; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DIOXYGENASES; MODELS, MOLECULAR; MUTAGENESIS; PHYLOGENY; POLYCHLORINATED BIPHENYLS; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SUBSTRATE SPECIFICITY;

PANDORAEA PNOMENUSA;

EID: 84871858759     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052550     Document Type: Article

References (54)

1. Carpenter DO, (2006) Polychlorinated Biphenyls (PCBs): Routes of Exposure and Effects on Human Health. Reviews on Environmental Health 21: 1.
2. Furukawa K, (2000) Biochemical and genetic bases of microbial degradation of polychlorinated biphenyls (PCBs). The Journal of General and Applied Microbiology 46: 283-296.
3. Erickson BD, Mondello FJ, (1992) Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400. J Bacteriol 174: 2903-2912.
4. Seto M, Kimbara K, Shimura M, Hatta T, Fukuda M, et al. (1995) A Novel Transformation of Polychlorinated Biphenyls by Rhodococcus sp. Strain RHA1. Appl Environ Microbiol 61: 3353-3358.
5. Vézina J, Barriault D, Sylvestre M, (2008) Diversity of the C-Terminal Portion of the Biphenyl Dioxygenase Large Subunit. Journal of Molecular Microbiology & Biotechnology 15: 139-151.
6. Kauppi B, Lee K, Carredano E, Parales RE, Gibson DT, et al. (1998) Structure of an aromatic-ring-hydroxylating dioxygenase- naphthalene 1,2-dioxygenase. Structure 6: 571-586.
7. Furusawa Y, Nagarajan V, Tanokura M, Masai E, Fukuda M, et al. (2004) Crystal structure of the terminal oxygenase component of biphenyl dioxygenase derived from Rhodococcus sp. strain RHA1. J Mol Biol 342: 1041-1052.
8. Ferraro D, Brown E, Yu C-L, Parales R, Gibson D, et al. (2007) Structural investigations of the ferredoxin and terminal oxygenase components of the biphenyl 2,3-dioxygenase from Sphingobium yanoikuyae B1. BMC Structural Biology 7: 10.
9. Kim E, Zylstra GJ, (1999) Functional analysis of genes involved in biphenyl, naphthalene, phenanthrene, and m-xylene degradation by Sphingomonas yanoikuyae B1. Journal of Industrial Microbiology and Biotechnology 23: 294-302.
10. Iwasaki T, Takeda H, Miyauchi K, Yamada T, Masai E, et al. (2007) Characterization of Two Biphenyl Dioxygenases for Biphenyl/PCB Degradation in A PCB Degrader, Rhodococcus sp. Strain RHA1. Bioscience, Biotechnology, and Biochemistry 71: 993-1002.
11. Furukawa K, Miyazaki T, (1986) Cloning of a gene cluster encoding biphenyl and chlorobiphenyl degradation in Pseudomonas pseudoalcaligenes. J Bacteriol 166: 392-398.
12. Erickson BD, Mondello FJ, (1993) Enhanced biodegradation of polychlorinated biphenyls after site-directed mutagenesis of a biphenyl dioxygenase gene. Appl Environ Microbiol 59: 3858-3862.
13. Gibson DT, Cruden DL, Haddock JD, Zylstra GJ, Brand JM, (1993) Oxidation of polychlorinated biphenyls by Pseudomonas sp. strain LB400 and Pseudomonas pseudoalcaligenes KF707. J Bacteriol 175: 4561-4564.
14. Kimura N, Nishi A, Goto M, Furukawa K, (1997) Functional analyses of a variety of chimeric dioxygenases constructed from two biphenyl dioxygenases that are similar structurally but different functionally. J Bacteriol 179: 3936-3943.
15. Mondello FJ, Turcich MP, Lobos JH, Erickson BD, (1997) Identification and modification of biphenyl dioxygenase sequences that determine the specificity of polychlorinated biphenyl degradation. Appl Environ Microbiol 63: 3096-3103.
16. Suenaga H, Watanabe T, Sato M, Ngadiman, Furukawa K, (2002) Alteration of Regiospecificity in Biphenyl Dioxygenase by Active-Site Engineering. J Bacteriol 184: 3682-3688.
17. Imbeault NYR, Powlowski JB, Colbert CL, Bolin JT, Eltis LD, (2000) Steady-state kinetic characterization and crystallization of a polychlorinated biphenyl-transforming dioxygenase. Journal of Biological Chemistry 275: 12430-12437.
18. Gomez-Gil L, Kumar P, Barriault D, Bolin JT, Sylvestre M, et al. (2007) Characterization of Biphenyl Dioxygenase of Pandoraea pnomenusa B-356 As a Potent Polychlorinated Biphenyl-Degrading Enzyme. J Bacteriol 189: 5705-5715.
19. Furukawa K, Suenaga H, Goto M, (2004) Biphenyl Dioxygenases: Functional Versatilities and Directed Evolution. J Bacteriol 186: 5189-5196.
20. Suenaga H, Mitsuoka M, Ura Y, Watanabe T, Furukawa K, (2001) Directed Evolution of Biphenyl Dioxygenase: Emergence of Enhanced Degradation Capacity for Benzene, Toluene, and Alkylbenzenes. J Bacteriol 183: 5441-5444.
21. Barriault D, Plante M-M, Sylvestre M, (2002) Family Shuffling of a Targeted bphA Region To Engineer Biphenyl Dioxygenase. J Bacteriol 184: 3794-3800.
22. Parales RE, Huang R, Yu C-L, Parales JV, Lee FKN, et al. (2005) Purification, Characterization, and Crystallization of the Components of the Nitrobenzene and 2-Nitrotoluene Dioxygenase Enzyme Systems. Appl Environ Microbiol 71: 3806-3814.
23. Habe H, Miyakoshi M, Chung J, Kasuga K, Yoshida T, et al. (2003) Phthalate catabolic gene cluster is linked to the angular dioxygenase gene in Terrabacter sp. strain DBF63. Applied Microbiology and Biotechnology 61: 44-54.
24. Nam J-W, Nojiri H, Yoshida T, Habe H, Yamane H, et al. (2001) New Classification System for Oxygenase Components Involved in Ring-Hydroxylating Oxygenations. Bioscience, Biotechnology, and Biochemistry 65: 254-263.
25. Kweon O, Kim SJ, Baek S, Chae JC, Adjei MD, et al. (2008) A new classification system for bacterial Rieske non-heme iron aromatic ring-hydroxylating oxygenases. BMC Biochem 9: 11.
26. Hirose J, Suyama A, Hayashida S, Furukawa K, (1994) Construction of hybrid biphenyl (bph) and toluene (tod) genes for functional analysis of aromatic ring dioxygenases. Gene 138: 27-33.
27. Hurtubise Y, Barriault D, Sylvestre M, (1998) Involvement of the terminal oxygenase beta subunit in the biphenyl dioxygenase reactivity pattern toward chlorobiphenyls. Journal of Bacteriology 180: 5828-5835.
28. Chebrou H, Hurtubise Y, Barriault D, Sylvestre M, (1999) Heterologous expression and characterization of the purified oxygenase component of Rhodococcus globerulus P6 biphenyl dioxygenase and of chimeras derived from it. Journal of Bacteriology 181: 4805-4811.
29. Parales RE, Emig MD, Lynch NA, Gibson DT, (1998) Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems. Journal of Bacteriology 180: 2337-2344.
30. Parales RE, Parales JV, Gibson DT, (1999) Aspartate 205 in the Catalytic Domain of Naphthalene Dioxygenase Is Essential for Activity. Journal of Bacteriology 181: 1831-1837.
31. Han S, Eltis LD, Timmis KN, Muchmore SW, Bolin JT, (1995) Crystal structure of the biphenyl-cleaving extradiol dioxygenase from a PCB-degrading pseudomonad. Science (Washington, D C) 270: 976-980.
32. Sugiyama K, Senda T, Narita H, Yamamoto T, Kimbara K, et al. (1995) 3-Dimensional structure of 2,3-dihydroxybiphenyl dioxygenase (BphC enzyme) from Pseudomonas sp strain-KKS102 having polychlorinated biphenyl (PCB)-degrading activity. Proceedings of the Japan Academy Series B- Physical and Biological Sciences 71: 32.
33. Goodwill KE, Sabatier C, Marks C, Raag R, Fitzpatrick PF, et al. (1997) Crystal structure of tyrosine hydroxylase at 2.3 Å and its implications for inherited neurodegenerative diseases. Nature Structural Biology 4: 578.
34. Boyington JC, Gaffney BJ, Amsel LM, (1993) The three-dimensional structure of an arachidonic acid 15-lipoxygenase. Science 260: 1482.
35. Dong X, Fushinobu S, Fukuda E, Terada T, Nakamura S, et al. (2005) Crystal structure of the terminal oxygenase component of cumene dioxygenase from Pseudomonas fluorescens IP01. J Bacteriol 187: 2483-2490.
36. Aoki H, Kimura T, Habe H, Yamane H, Kodama T, et al. (1996) Cloning, nucleotide sequence, and characterization of the genes encoding enzymes involved in the degradation of cumene to 2-hydroxy-6-oxo-7-methylocta-2,4-dienoic acid in Pseudomonas fluorescens IP01. Journal of Fermentation and Bioengineering 81: 187-196.
37. Martins BM, Svetlitchnaia T, Dobbek H, (2005) 2-Oxoquinoline 8-monooxygenase oxygenase component: active site modulation by Rieske-[2Fe-2S] center oxidation/reduction. Structure 13: 817-824.
38. Karlsson A, Parales JV, Parales RE, Gibson DT, Eklund H, et al. (2003) Crystal Structure of Naphthalene Dioxygenase: Side-on Binding of Dioxygen to Iron. Science 299: 1039-1042.
39. Dai S, Vaillancourt FH, Maaroufi H, Drouin NM, Neau DB, et al. (2002) Identification and analysis of a bottleneck in PCB biodegradation. Nat Struct Mol Biol 9: 934-939.
40. Zielinski M, Kahl S, Hecht H-J, Hofer B, (2003) Pinpointing Biphenyl Dioxygenase Residues That Are Crucial for Substrate Interaction. J Bacteriol 185: 6976-6980.
41. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-4680.
42. Clamp M, Cuff J, Searle SM, Barton GJ, (2004) The Jalview Java alignment editor. Bioinformatics 20: 426-427.
43. Felsenstein J, (1989) PHYLIP- Phylogeny Inference Package (Version 3.2). Cladistics 5: 164-166.
44. Otwinowski Z, Minor W, (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods in Enzymology 276: 307-326.
45. Collaborative Computational Project Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D50: 760-763.
46. Howells ER, Phillips DC, Rogers D, (1950) The probability distribution of X-ray intensities. II. Experimental investigation and the X-ray detection of centres of symmetry. Acta Crystallographica 3: 210-214.
47. Rees D, (1980) The influence of twinning by merohedry on intensity statistics. Acta Crystallographica Section A 36: 578-581.
48. Wilson K, French S, (1978) On the treatment of negative intensity observations. Acta Crystallographica A34: 517-525.
49. Yeates TO, (1997) Detecting and overcoming crystal twinning. Methods in Enzymology 276: 13-22.
50. Navaza J, (1994) AMoRe - an automated package for molecular replacement. Acta Crystallographica A50: 157-163.
51. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallographica D54: 905-921.
52. Jones TA, Zou JY, Cowan SW, Kjeldgaard M, (1991) Improved methods for building protein models in electron density maps and the location of error in these models. Acta Crystallographica A47: 110-119.
53. Sheldrick GM, Schneider TR, (1997) SHELXL: high resolution refinement. Methods in Enzymology 277: 319-343.
54. Murshudov GN, Vagin AA, Dodson E (1996) Application of maximum-likelihood refinement. Refinement of protein structures, proceedings of Daresbury study weekend. Warrington: Daresbury Laboratory.