Structural, Biochemical and Genetic Characterization of Dissimilatory ATP Sulfurylase from Allochromatium vinosum

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Parey, Kristian ^a,b   Demmer, Ulrike ^a   Warkentin, Eberhard ^a   Wynen, Astrid ^c   Ermler, Ulrich ^a   Dahl, Christiane ^c  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE 5' PHOSPHOSULFATE; PYROPHOSPHATE; RECOMBINANT ENZYME; SULFATE ADENYLYLTRANSFERASE;

ALLOCHROMATIUM VINOSUM; APRMBA GENE; ARTICLE; BACTERIAL GENE; CHROMATIACEAE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; GENE INACTIVATION; GENE INSERTION; GENE LOCUS; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHOTOTROPHIC BACTERIUM; PROTEIN FAMILY; SAT GENE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; SULFUR BACTERIUM; SULFUR OXIDIZING BACTERIUM;

ADENOSINE PHOSPHOSULFATE; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHROMATIACEAE; DIPHOSPHATES; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SULFATE ADENYLYLTRANSFERASE; SULFATES;

EID: 84884484623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074707     Document Type: Article

References (51)

1. Schwenn JD (1997) Assimilatory reduction of inorganic sulphate. In: Cram WJ, et al., editors. Sulphur metabolism in higher plants. Leiden: Backhuys Publishers. 39-57.
2. Hansen TA, (1994) Metabolism of sulfate-reducing prokaryotes. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 66: 165-185.
3. Hipp WM, Pott AS, Thum-Schmitz N, Faath I, Dahl C, et al. (1997) Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes. Microbiology 143: 2891-2902.
4. Dahl C, Trüper HG, (1994) Enzymes of dissimilatory sulfide oxidation in phototrophic bacteria. Meth Enzymol 243: 400-421.
5. Postgate JR (1984) The sulphate reducing bacteria. Cambridge: Cambridge University Press.
6. Friedrich CG, (1998) Physiology and genetics of sulfur-oxidizing bacteria. Adv Microb Physiol 39: 235-289.
7. Fritz G, Einsle O, Rudolf M, Schiffer A, Kroneck PMH, (2005) Key bacterial multi-centered metal enzymes involved in nitrate and sulfate respiration. J Mol Microbiol Biotechnol 10: 223-233.
8. Patron NJ, Durnford DG, Kopriva S, (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol Biol 8: 39.
9. Leyh TS, Taylor JC, Markham GD, (1988) The sulfate acitvation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J Biol Chem 263: 2409-2416.
10. Karamohamed S, Nilsson J, Nourizad K, Ronaghi M, Pettersson B, et al. (1999) Production, purification, and luminometric analysis of recombinant Saccharomyces cerevisiae MET3 adenosine triphosphate sulfurylase expressed in Escherichia coli. Protein Expr Purif 15: 381-388.
11. Foster BA, Thomas SM, Mahr JA, Renosto F, Patel HC, et al. (1994) Cloning and sequencing of ATP sulfurylase from Penicillium chrysogenum: Identification of a likely allosteric domain. J Biol Chem 269: 19777-19786.
12. Renosto F, Martin RL, Borrell JL, Nelson DC, Segel IH, (1991) ATP sulfurylase from trophosome tissue of Riftia pachyptila (hydrothermal vent tube worm). Arch Biochem Biophys 290: 66-78.
13. Logan HM, Cathala N, Grignon C, Davidian JC, (1996) Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfurylase multigene family- Expression studies in yeast and in relation to plant sulfur nutrition. J Biol Chem 271: 12227-12233.
14. MacRae IJ, Segel IH, Fisher AJ, (2001) Crystal structure of ATP sulfurylase from Penicillium chrysogenum: Insights into the allosteric regulation of sulfate assimilation. Biochemistry 40: 6795-6804.
15. Hanna E, MacRae IJ, Medina DC, Fisher AJ, Segel IH, (2002) ATP sulfurylase from the hyperthermophilic chemolithotroph Aquifex aeolicus. Arch Biochem Biophys 406: 275-288.
16. Li H, Deyrup A, Mensch JR, Domowicz M, Konstantinidis AK, et al. (1995) The isolation and characterization of cDNA encoding the mouse bifunctional ATP sulfurylase-adenosine 5′-phosphosulfate kinase. J Biol Chem 270: 29453-29459.
17. Gavel OY, Bursakov SA, Calvete JJ, George GN, Moura JJG, et al. (1998) ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing cobalt and zinc. Biochemistry 37: 16225-16232.
18. Weissgerber T, Zigann R, Bruce D, Chang Y-J, Detter JC et al. (2011) Complete genome sequence of Allochromatium vinosum DSM 180T. Stand Genomic Sci 5: doi:10.4056/sigs.2335270.
19. Neumann S, Wynen A, Trüper HG, Dahl C, (2000) Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway. Mol Biol Reports 27: 27-33.
20. Meyer B, Kuever J, (2007) Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5′-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology 153: 3478-3498.
21. Gregersen LH, Bryant DA, Frigaard N-U (2011) Mechanisms and evolution of oxidative sulfur metabolism in green sulfur bacteria. Front Microbiol 2: 116-doi: 10.3389/fmicb.2011.00116.
22. Pires RH, Lourenco AI, Morais F, Teixeira M, Xavier AV, et al. (2003) A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim Biophys Acta 1605: 67-82.
23. Ramos AR, Keller KL, Wall JD, Pereira IA, (2012) The membrane QmoABC complex interacts directly with the dissimilatory adenosine 5′-phosphosulfate reductase in sulfate reducing bacteria. Front Microbiol 3: 137.
24. Frigaard N-U, Dahl C, (2009) Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol 54: 103-200.
25. Rodriguez J, Hiras J, Hanson TE (2011) Sulfite oxidation in Chlorobaculum tepidum. Front Microbiol 2: 112-doi: 10.3389/fmcib.2011.00112.
26. Dahl C, (1996) Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. Microbiology 142: 3363-3372.
27. Sanchez O, Ferrera I, Dahl C, Mas J, (2001) In vivo role of APS reductase in the purple sulfur bacterium Allochromatium vinosum. Arch Microbiol 176: 301-305.
28. Ullrich TC, Blaesse M, Huber R, (2001) Crystal structure of ATP sulfurylase from Saccharomyces cerevisiae, a key enzyme in sulfate activation. EMBO J 20: 316-329.
29. Yu Z, Lansdon EB, Segel IH, Fisher AJ, (2007) Crystal structure of the bifunctional ATP sulfurylase- APS kinase from the chemolithotrophic thermophile Aquifex aeolicus. J Mol Biol 365: 732-743.
30. Beynon JD, MacRae IJ, Huston SL, Nelson DC, Segel IH, et al. (2001) Crystal structure of ATP sulfurylase from the bacterial symbiont of the hydrothermal vent tubeworm Riftia pachyptila. Biochemistry 40: 14509-14517.
31. Harjes S, Bayer P, Scheidig AJ, (2005) The crystal structure of human PAPS synthetase 1 reveals asymmetry in substrate binding. J Mol Biol 347: 623-635.
32. Taguchi Y, Sugishima M, Fukuyama K, (2004) Crystal structure of a novel zinc-binding ATP sulfurylase from Thermus thermophilus HB8. Biochemistry 43: 4111-4118.
33. Ullrich TC, Huber R, (2001) The complex structures of ATP sulfurylase with thiosulfate, ADP and chlorate reveal new insights in inhibitory effects and the catalytic cycle. J Mol Biol 313: 1117-1125.
34. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, et al. (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 30: 2785-2791.
35. Seubert PA, Renosto F, Knudson P, Segel IH, (1985) Adenosinetriphosphate sulfurylase from Penicillium chrysogenum: steady-state kinetics of the forward and reverse reactions, alternative substrate kinetics, and equilibrium binding studies. Arch Biochem Biophys 240: 509-523.
36. Venkatachalam KV, Fuda H, Koonin EV, Strott CA, (1999) Site-selected mutagenesis of a conserved nucleotide binding HXGH motif located in the ATP sulfurylase domain of human bifunctional 3′-phosphoadenosine 5′-phosphosulfate synthase. J Biol Chem 274: 2601-2604.
37. Deyrup AT, Singh B, Krishnan S, Lyle S, Schwartz NB, (1999) Chemical modification and site-directed mutagenesis of conserved HXXH and PP-loop motif arginines and histidines in the murine bifunctional ATP sulfurylase/adenosine 5′-phosphosulfate kinase. J Biol Chem 274: 28929-28936.
38. Holm L, Sander C, (1993) Protein structure comparison by alignment of distance matrices. J Mol Biol 233: 123-138.
39. Simon R, Priefer U, Pühler A, (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1: 784-791.
40. Fellay R, Frey J, Krisch HM, (1987) Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vivo insertional mutagenesis of Gram-negative bacteria. Gene 52: 147-154.
41. Pattaragulwanit K, Dahl C, (1995) Development of a genetic system for a purple sulfur bacterium: conjugative plasmid transfer in Chromatium vinosum. Arch Microbiol 164: 217-222.
42. Segel IH, Renosto F, Seubert PA, (1987) Sulfate-activating enzymes. Meth Enzymol 143: 334-349.
43. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Meth Enzymol 276: 307-326.
44. Kissinger CR, Gehlhaar DK, Fogel DB, (1999) Rapid automated molecular replacement by evolutionary search. Acta Crystallogr D Biol Crystallogr 55: 484-491.
45. Jones TA, Zou JY, Cowan SW, Kjeldgaard M, (1991) Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119.
46. Brunger AT, Adams PD, Clore GM, Delano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
47. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
48. Potterton E, McNicholas S, Krissinel E, Cowtan K, Noble M, (2002) The CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 58: 1955-1957.
49. Brunger AT, (1992) Free R-value- a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355: 472-475.
50. Thompson JD, Gibson TJ, Plewniak F, Higgins DG, (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24: 4876-4882.
51. Gouet P, Courcelle E, Stuart DI, Metoz F, (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.