The Respiratory Arsenite Oxidase: Structure and the Role of Residues Surrounding the Rieske Cluster

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Warelow, Thomas P ^a   Oke, Muse ^b   Schoepp Cothenet, Barbara ^c   Dahl, Jan U ^d   Bruselat, Nicole ^a   Sivalingam, Ganesh N ^a   Leimkühler, Silke ^d   Thalassinos, Konstantinos ^a   Kappler, Ulrike ^e   Naismith, James H ^b   Santini, Joanne M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d UNIVERSITY OF POTSDAM   (Germany)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; ARSENITE OXIDASE; HETERODIMER; OXIDOREDUCTASE; RECOMBINANT PROTEIN; SERINE; THREONINE; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

AIOA GENE; AIOB GENE; ALCALIGENES FAECALIS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BETAPROTEOBACTERIA; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; ENZYME SUBUNIT; ESCHERICHIA COLI; GENE FUNCTION; GENETIC CONSERVATION; HETEROLOGOUS EXPRESSION; MOLECULAR CLONING; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PROTEIN STABILITY; RESIDUE ANALYSIS; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; SPECIES DIFFERENCE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

AEROBIOSIS; ALCALIGENES FAECALIS; ALPHAPROTEOBACTERIA; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT COMPLEX III; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLYBDENUM; MUTANT PROTEINS; MUTATION; OXIDATION-REDUCTION; OXIDOREDUCTASES; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84883383174     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072535     Document Type: Article

References (45)

1. Santini JM, Sly LI, Schnagl RD, Macy JM (2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a goldmine: phylogenetic, physiological and preliminary biochemical studies. Appl. Environ. Microbiol. 66, 92-97.
2. Lett M-C, Muller D, Lièvremont D, Silver S, Santini JM (2012) Unified nomenclature for genes involved in prokaryotic aerobic arsenite oxidation. J. Bacteriol. 194, 207-208.
3. van Lis R, Nitschke W, Duval S, Schoepp-Cothenet B (2012) Evolution of arsenite oxidation. In Metabolism of Arsenite (Santini, J. M. and Ward, S. A. ed.), chapter 10, 125-144, CRC Press, London.
4. van Lis R, Nitschke W, Duval S, Schoepp-Cothenet B (2012) Arsenics as bioenergetic substrates. Biochim. Biophys. Acta. doi:10.1016/j.bbabio.2012.08.007.
5. Santini JM, vanden Hoven RN (2004) Molybdenum-containing arsenite oxidase from the chemolithoautotrophic arsenite oxidizer NT-26. J. Bacteriol. 186, 1614-1619.
6. Ellis PJ, Conrads T, Hille R, Kuhn P (2001) Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 A ° and 2.03 A °. Structure 9, 125-132.
7. Romão MJ (2009) Molybdenum and tungsten enzymes: a crystallographic and mechanistic overview. Dalton Trans. 21, 4053-4068.
8. Anderson G, Williams J, Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J. Biol. Chem. 267, 23674-23682.
9. Lieutaud A, van Lis R, Duval S, Capowiez L, Muller D, et al. (2010) Arsenite oxidase from Ralstonia sp. 22: characterization of the enzyme and its interaction with soluble cytochromes. J. Biol. Chem. 285, 20433-20441.
10. Santini JM, Kappler U, Ward SA, Honeychurch MJ, vanden Hoven RN, et al. (2007) The NT-26 cytochrome c552 and its role in arsenite oxidation. Biochim. Biophys. Acta 1767, 189-196.
11. vanden Hoven RN, Santini JM (2004) Arsenite oxidation by the heterotroph Hydrogenophaga sp. str. NT-14: the arsenite oxidase and its physiological electron acceptor. Biochim. Biophys. Acta 1656, 148-155.
12. Duval S, Santini JM, Nitschke W, Hille R, Schoepp-Cothenet B (2010) The small subunit AroB of arsenite oxidase: lessons on the (2Fe-2S)-Rieske protein superfamily. J. Biol. Chem. 285, 20442-20451.
13. Hoke KR, Cobb N, Armstrong FA, Hille R (2004) Electrochemical studies of arsenite oxidase: an unusual example of a highly cooperative two-electron molybdenum center. Biochemistry 43, 1667-1674.
14. Guergova-Kuras M, Kuras R, Ugulava N, Hadad I, Crofts AR (2000) Specific mutagenesis of the Rieske iron-sulphur protein in Rhodobacter sphaeroides shows that both the thermodynamic gradient and the pK of the oxidised form determine the rate of quinol oxidation by the bc1 complex. Biochemistry 39, 7436-7444.
15. Kolling DJ, Brunzelle JS, Lhee S, Crofts AR, Nair SK (2007) Atomic resolution structures of Rieske iron-sulphur protein: role of hydrogen bonds in tuning the redox potential of the iron-sulphur clusters. Structure 15, 19-38.
16. Leggate EJ, Hirst J (2005) Roles of the disulfide bond and adjacent residues in determining the reduction potentials and stabilities of respiratory-type Rieske clusters. Biochemistry 44, 7048-7058.
17. Lhee S, Kolling DR, Nair SK, Dikanov SA, Crofts AR (2010) Modifications of protein environment of the (2Fe-2S) cluster of the bc1 complex: effects on the biophysical properties of the Rieske iron-sulfur protein and on the kinetics of the complex. J. Biol. Chem. 285, 9233-9248.
18. Mertitz-Zahradnik T, Zwicker K, Nett JH, Link TA, Trumpower BL (2003) Elimination of the disulfide bridge in the Rieske iron-sulphur protein allows assembly of the (2Fe-2S) cluster into the Rieske protein but damages the ubiquinol oxidation site in the cytochrome bc1 complex. Biochemistry 42, 13637-13645.
19. Hanahan D (1984) Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580.
20. Yanisch-Perron C, Vieria J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.
21. Stewart VJ, MacGregor CH (1982) Nitrate reductase in Escherichia coli K-12: involvement of chlC, chlE, and chlG loci. J. Bacteriol. 151, 788-799.
22. Miroux B, Walker JE (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298.
23. Osborne TH, Heath MD, Martin ACR, Pankowski JA, Hudson-Edwards KA, et al. (2012) Cold-adapted arsenite oxidase from a psychrotolerant Polaromonas species. Metallomics 5, 318-324.
24. Edelhoch H (1967) Spectroscopic Determination of Tryptophan and Tyrosine in Proteins Biochemistry, 6, 1948-1956.
25. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T (1995), How to measure and predict the molar absorption coefficient of a protein. Protein Sci., 11, 2411-2423.
26. Pringle SD, Giles K, Wildgoose JL, Williams JP, Slade SE, et al. (2007) An investigation of the mobility separation of some peptide and protein ions using a new hybrid quadrupole/travelling wave IMS/oa-ToF instrument. Internat. J. Mass Spec. 261, 1-12.
27. Evans PR (1997) Scaling of X-ray data. Newsletter on Protein Crystallography 33, 22-24.
28. Leslie AGW (1992) Recent Developments in MOSFLM. Joint CCP4 and ESF-EAMCB newsletter on protein crystallography, No 26, 1-10.
29. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ (2005) Likelihood-enhanced fast translation functions. Acta Cryst. D61, 458-464.
30. Storoni LC, McCoy AJ, Read RJ (2004) Likelihood-enhanced fast rotation functions. Acta Cryst. D60, 432-438.
31. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Cryst. D50, 760-763.
32. Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Cryst. D62, 1002-1011.
33. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Cryst. D60, 2126-2132.
34. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of Macromolecular Structures by the Maximum-Likelihood Method. Acta Cryst. D53, 240-255.
35. Winn MD, Murshudov GN, Papiz MZ (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321.
36. Painter J, Merritt EA (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Cryst. 39, 109-111.
37. Dutton PL (1971) Oxidation-reduction potential dependence of the interaction of cytochromes, bacteriochlorophyll and carotenoids at 77 degrees K in chromatophores of Chromatium D and Rhodopseudomonas gelatinosa. Biochim. Biophys. Acta 226, 63-80.
38. Lebrun E, Brugna M, Baymann F, Muller D, Lièvremont D, et al. (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol. Biol. Evol. 20, 686-693.
39. Krissinel E, Henrick K (2005) Detection of protein assemblies in crystals. Computational Life Sciences, Proceedings 3695, 163-174.
40. Liebl U, Sled V, Brasseur G, Ohnishi T, Daldal F (1997) Conserved non liganding residues of the Rhodobacter capsulatus Rieske iron-sulfur protein of the bc1 complex are essential for protein structure, properties of the (2Fe-2S) cluster, and communication with the quinone pool. Biochemistry. 36, 11675-11684.
41. Davidson E, Ohnishi T, Atta-Asafo-Adeji E, Daldal F (1992) Potential ligands to the (2Fe-2S) Rieske cluster of the cytochrome bc1 complex of Rhodobacter capsulatus probed by site-directed mutagenesis. Biochemistry 31, 3342-3351.
42. van Lis R, Nitschke W, Warelow TP, Capowiez L, Santini JM, et al. (2012) Heterologously expressed arsenite oxidase: a system to study biogenesis and structure/function relationships of the enzyme family. Biochim. Biophys. Acta 1817, 1701-1708.
43. Hilton JC, Temple CA, Rajagopalan KV (1999) Re-design of Rhodobacter sphaeroides dimethyl sulfoxide reductase. Enhancement of adenosine N1-oxide reductase activity. J. Biol. Chem. 274, 8428-8436.
44. Temple CA, George GN, Hilton JC, George MJ, Prince RC, et al. (2000) Structure of the molybdenum site of Rhodobacter sphaeroides biotin sulfoxide reductase. Biochemistry 39, 4046-4052.
45. Denke E, Merbitz-Zahradnik T, Hatzfeld OM, Snyder CH, Link TA, et al. (1998) Alteration of the midpoint potential and catalytic activity of the Rieske iron-sulfur protein by changes of amino acids forming hydrogen bonds to the iron-sulfur cluster. J. Biol. Chem. 273, 9085-9093.