Molybdenum incorporation in tungsten aldehyde oxidoreductase enzymes from Pyrococcus furiosus

Journal of Bacteriology

Volumn 192, Issue 16, 2010, Pages 4143-4152

  Sevcenco, Ana Maria ^a   Bevers, Loes E ^a,b   Pinkse, Martijn W H ^a   Krijger, Gerard C ^a,c   Wolterbeek, Hubert T ^a   Verhaert, Peter D E M ^a   Hagen, Wilfred R ^a   Hagedoorn, Peter Leon ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ALDEHYDE; ALDEHYDE DEHYDROGENASE; CROTONALDEHYDE; FERREDOXIN OXIDOREDUCTASE; FORMALDEHYDE; GLYCERALDEHYDE 3 PHOSPHATE; MOLYBDENUM; MOLYBDENUM 99; MOLYBDIC ACID; MOLYBDOPTERIN; TUNGSTEN; TUNGSTEN CONTAINING OXIDOREDUCTASE 4; TUNGSTEN CONTAINING OXIDOREDUCTASE 5; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; RADIOISOTOPE;

ARTICLE; AUTORADIOGRAPHY; BACTERIAL GROWTH; CORRELATION ANALYSIS; CULTURE MEDIUM; ELECTRON SPIN RESONANCE; HYPERTHERMOPHILIC ARCHAEON; NEGATIVE FEEDBACK; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PYROCOCCUS FURIOSUS; COENZYME; ENZYMOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; STAINING;

ARCHAEA; PYROCOCCUS FURIOSUS;

ALDEHYDE OXIDOREDUCTASES; ARCHAEAL PROTEINS; AUTORADIOGRAPHY; COENZYMES; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MOLYBDENUM; OXIDATION-REDUCTION; PYROCOCCUS FURIOSUS; RADIOISOTOPES; STAINING AND LABELING; TUNGSTEN;

EID: 77955947485     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00270-10     Document Type: Article

References (33)

1. Anderson, L. A., T. Palmer, N. C. Price, S. Bornemann, D. H. Boxer, and R. N. Pau. 1997. Characterisation of the molybdenum-responsive ModE regulatory protein and its binding to the promoter region of the modABCD (molybdenum transport) operon of Escherichia coli. Eur. J. Biochem. 246: 119-126.
2. Arendsen, A. F., P. T. M. Veenhuizen, and W. R. Hagen. 1995. Redox properties of the sulfhydrogenase from Pyrococcus furiosus. FEBS Lett. 368:117-121.
3. Bevers, L. E., E. Bol, P. L. Hagedoorn, and W. R. Hagen. 2005. WOR5: a novel tungsten containing aldehyde oxidoreductase from Pyrococcus furiosus with a broad substrate specificity. J. Bacteriol. 187:7056-7061.
4. Bevers, L. E., P. L. Hagedoorn, G. C. Krijger, and W. R. Hagen. 2006. Tungsten transport protein A (WtpA) in Pyrococcus furiosus: first member of a new class of tungstate and molybdate transporters. J. Bacteriol. 188:6498-6505.
5. Bevers, L. E., P. L. Hagedoorn, J. A. Santamaria-Araujo, A. Magalon, W. R. Hagen, and G. Schwarz. 2008. A function for MoaB in the biosynthesis of the molybdenum and tungsten cofactors. Biochemistry 47:949-956.
6. Bevers, L. E., and W. R. Hagen. 2009. One- and two-electron reduction of molybdate reversibly bound to the archaeal tungstate/molybdate transporter WtpA. Dalton Trans. 2009(39):8168-8170.
7. Bol, E., L. E. Bevers, P. L. Hagedoorn, and W. R. Hagen. 2006. Redox chemistry of tungsten and iron-sulfur prosthetic groups in Pyrococcus furiosus formaldehyde ferredoxin oxidoreductase. J. Biol. Inorg. Chem. 11:999-1006.
8. Bursakov, S. A., O. Y. Gavel, G. Di Rocco, J. Lampreia, J. Calvete, A. S. Pereira, J. J. G. Moura, and I. Moura. 2004. Antagonists Mo and Cu in a heterometallic cluster present on a novel protein (orange protein) isolated from Desulfovibrio gigas. J. Inorg. Biochem. 98:833-840.
9. Falia, G., and K. O. Stetter. 1986. Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaeabacteria growing optimally at 100°C. Arch. Microbiol. 145:56-61.
10. Gerber, S., M. Comellas-Bigler, B. A. Goetz, and K. P. Locher. 2008. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 321:246-250.
11. Grunden, A. M., R. M. Ray, J. K. Rosentel, F. G. Healy, and K. T. Shanmugam. 1996. Repression of the Escherichia coli modABCD (molybdate transport) operon by ModE. J. Bacteriol. 178:735-744.
12. Grunden, A. M., and K. T. Shanmugam. 1997. Molybdate transport and regulation in bacteria. Arch. Microbiol. 168:345-354.
13. 235. Phys. Rev. 107:1642-1645.
14. Hagedoorn, P. L., P. Van 't Slot, H. P. Van Leeuwen, and W. R. Hagen. 2001. Electroanalytical determination of tungsten and molybdenum in proteins. Anal. Biochem. 297:71-78.
15. Llamas, A., T. Otte, A. Simons, G. Multhaup, R. R. Mendel, and G. Schwarz. 2006. The mechanism of nucleotide-assisted molybdenum insertion into molybdopterin: a novel route towards metal cofactor assembly. J. Biol. Chem. 281:18343-18350.
16. Martins, L. O., and H. Santos. 1995. Accumulation of mannosylglycerate and di-myo-inositol-phosphate by Pyrococcus furiosus in response to salinity and temperature. Appl. Environ. Microbiol. 61:3299-3303.
17. Mukund, S., and M. W. W. Adams. 1995. Glyceraldehyde-3-phosphate ferredoxin oxidoreductase, a novel tungsten-containing enzyme with a potential glycolytic role in the hyperthermophilic archaeon Pyrococcus furiosus. J. Biol. Chem. 270:8389-8392.
18. Mukund, S., and M. W. W. Adams. 1996. Molybdenum and vanadium do not replace tungsten in the catalytically active forms of the three tungstoenzymes in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 178:163-167.
19. Mukund, S., and M. W. W. Adams. 1991. The novel tungsten-iron-sulfur protein of the hyperthermophilic archaebacterium, Pyrococcus furiosus, is an aldehyde ferredoxin oxidoreductase. J. Biol. Chem. 266:14208-14216.
20. Overeijnder, M. L., W. R. Hagen, and P. L. Hagedoorn. 2009. A thermostable hybrid cluster protein from Pyrococcus furiosus: effects of the loss of a three helix bundle subdomain. J. Biol. Inorg. Chem. 14:703-710.
21. Raven, N., N. Ladwa, D. Cossar, and R Sharp. 1992. Continuous culture of the hyperthermophilic archaeum Pyrococcus furiosus. Appl. Microbiol. Biotechnol. 38:263-267.
22. Regulski, E. E., R. H. Moy, Z. Weinberg, J. E. Barrick, Z. Yao, W. L. Ruzzo, and R. R. Breaker. 2008. A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Mol. Microbiol. 68:918-932.
23. Robb, F. T., D. L. Maeder, J. R. Brown, J. DiRuggiero, M. D. Stump, R. K. Yeh, R. B. Weiss, and D. M. Dunn. 2001. Genomic sequence of hyperthermophile, Pyrococcus furiosus: implications for physiology and enzymology. Methods Enzymol. 330:134-157.
24. Roy, R., and M. W. W. Adams. 2002. Characterization of a fourth tungsten-containing enzyme from the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 184:6952-6956.
25. Roy, R., S. Mukund, G. J. Shut, D. M. Dunn, R. Weiss, and M. W. W. Adams. 1999. Purification and molecular characterization of the tungsten-containing formaldehyde ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus: the third of a putative five-member tungstoenzyme family. J. Bacteriol. 181:1171-1180.
26. Sapra, R., K. Bagramyan, and M. W. W. Adams. 2003. A simple energy-conserving system: proton reduction coupled to proton translocation. Proc. Natl. Acad. Sci. U. S. A. 100:7545-7550.
27. Sevcenco, A. M., G. C. Krijger, M. W. Pinkse, P. D. E. M. Verhaert, W. R. Hagen, and P. L. Hagedoorn. 2009. Development of a generic approach to native metalloproteomics: application to the quantitative identification of soluble copper proteins in Escherichia coli. J. Biol. Inorg. Chem. 14:631-640.
28. Sevcenco, A. M., M. W. Pinkse, E. Bol, G. C. Krijger, H. T. Wolterbeek, P. D. E. M. Verhaert, P. L. Hagedoorn, and W. R. Hagen. 2009. The tungsten metallome of Pyrococcus furiosus. Metallomics 1:395-402.
29. Smart, J. P., M. J. Cliff, and D. J. Kelly. 2009. A role for tungsten in the biology of Campylobacter jejuni: tungstate stimulates formate dehydrogenase activity and is transported via an ultra-high affinity ABC system distinct from the molybdate transporter. Mol. Microbiol. 74:742-757.
30. Taveirne, M. E., M. L. Sikes, and J. W. Olson. 2009. Molybdenum and tungsten in Campylobacter jejuni: their physiological role and identification of separate transporters regulated by a single ModE-like protein. Mol. Microbiol. 74:758-771.
31. van der Oost, J., G. J. Schut, S. W. M. Kengen, W. R. Hagen, M. Thomm, and W. M. de Vos. 1998. The ferredoxin-dependent conversion of glyceraldehyde- 3-phosphate in the hyperthermophilic archaeon Pyrococcus furiosus represents a novel site of glycolytic regulation. J. Biol. Chem. 273:28149-28154.
32. Weinberg, M. V., G. J. Schut, S. D. Brehm, S. Datta, and M. W. W. Adams. 2005. Cold shock of a hyperthermophilic archaeon: Pyrococcus furiosus exhibits multiple responses to a suboptimal growth temperature with a key role for membrane-bound glycoproteins. J. Bacteriol. 187:336-348.
33. Wilm, M., A. Schevchenko, T. Houthaeve, S. Breit, L. Schweigerer, T. Fotsis, and M. Mann. 1996. Femtomole sequencing of proteins form polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379:466-469.