1887

Abstract

Certain heavy metal ions such as copper and zinc serve as essential cofactors of many enzymes, but are toxic at high concentrations. Thus, intracellular levels have to be subtly balanced. P-type ATPases of the P-subclass play a major role in metal homeostasis. The thermoacidophile possesses two P-ATPases named CopA and CopB. Both enzymes are present in cells grown in copper-depleted medium and are accumulated upon an increase in the external copper concentration. We studied the physiological roles of both ATPases by disrupting genes and . Neither of them affected the sensitivity of to reactive oxygen species, nor were they a strict prerequisite to the biosynthesis of the copper protein cytochrome oxidase. Deletion mutant analysis demonstrated that CopA is an effective copper pump at low and high copper concentrations. CopB appeared to be a low-affinity copper export ATPase, which was only relevant if the media copper concentration was exceedingly high. CopA and CopB thus act as resistance factors to copper ions at overlapping concentrations. Moreover, growth tests on solid media indicated that both ATPases are involved in resistance to silver.

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2012-06-01
2024-03-28
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References

  1. Albers S. V., Driessen A. J. ( 2008). Conditions for gene disruption by homologous recombination of exogenous DNA into the Sulfolobus solfataricus genome. Archaea 2:145–149 [View Article][PubMed]
    [Google Scholar]
  2. Argüello J. M., Eren E., González-Guerrero M. ( 2007). The structure and function of heavy metal transport PIB-ATPases. Biometals 20:233–248 [View Article][PubMed]
    [Google Scholar]
  3. Argüello J. M., González-Guerrero M., Raimunda D. ( 2011). Bacterial transition metal P(IB)-ATPases: transport mechanism and roles in virulence. Biochemistry 50:9940–9949 [View Article][PubMed]
    [Google Scholar]
  4. Axelsen K. B., Palmgren M. G. ( 1998). Evolution of substrate specificities in the P-type ATPase superfamily. J Mol Evol 46:84–101 [View Article][PubMed]
    [Google Scholar]
  5. Balasubramanian R., Kenney G. E., Rosenzweig A. C. ( 2011). Dual pathways for copper uptake by methanotrophic bacteria. J Biol Chem 286:37313–37319 [View Article][PubMed]
    [Google Scholar]
  6. Baliga N. S., Bonneau R., Facciotti M. T., Pan M., Glusman G., Deutsch E. W., Shannon P., Chiu Y., Weng R. S. et al. ( 2004). Genome sequence of Haloarcula marismortui: a halophilic archaeon from the Dead Sea. Genome Res 14:2221–2234 [View Article][PubMed]
    [Google Scholar]
  7. Banci L., Bertini I., Cavallaro G., Ciofi-Baffoni S. ( 2011). Seeking the determinants of the elusive functions of Sco proteins. FEBS J 278:2244–2262 [View Article][PubMed]
    [Google Scholar]
  8. Brenner A. J., Harris E. D. ( 1995). A quantitative test for copper using bicinchoninic acid. Anal Biochem 226:80–84 [View Article][PubMed]
    [Google Scholar]
  9. Brock T. D., Brock K. M., Belly R. T., Weiss R. L. ( 1972). Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol 84:54–68 [View Article][PubMed]
    [Google Scholar]
  10. Cannio R., D’angelo A., Rossi M., Bartolucci S. ( 2000). A superoxide dismutase from the archaeon Sulfolobus solfataricus is an extracellular enzyme and prevents the deactivation by superoxide of cell-bound proteins. Eur J Biochem 267:235–243 [View Article][PubMed]
    [Google Scholar]
  11. Carr H. S., Maxfield A. B., Horng Y. C., Winge D. R. ( 2005). Functional analysis of the domains in Cox11. J Biol Chem 280:22664–22669 [View Article][PubMed]
    [Google Scholar]
  12. Chen L., Brügger K., Skovgaard M., Redder P., She Q., Torarinsson E., Greve B., Awayez M., Zibat A. et al. ( 2005). The genome of Sulfolobus acidocaldarius, a model organism of the Crenarchaeota. J Bacteriol 187:4992–4999 [View Article][PubMed]
    [Google Scholar]
  13. Coombs J. M., Barkay T. ( 2005). New findings on evolution of metal homeostasis genes: evidence from comparative genome analysis of bacteria and archaea. Appl Environ Microbiol 71:7083–7091 [View Article][PubMed]
    [Google Scholar]
  14. de Rosa M., Gambacorta A., Bu’lock J. D. ( 1975). Extremely thermophilic acidophilic bacteria convergent with Sulfolobus acidocaldarius . J Gen Microbiol 86:156–164[PubMed] [CrossRef]
    [Google Scholar]
  15. Deigweiher K., Drell T. L. IV, Prutsch A., Scheidig A. J., Lübben M. ( 2004). Expression, isolation, and crystallization of the catalytic domain of CopB, a putative copper transporting ATPase from the thermoacidophilic archaeon Sulfolobus solfataricus . J Bioenerg Biomembr 36:151–159 [View Article][PubMed]
    [Google Scholar]
  16. Ettema T. J., Huynen M. A., de Vos W. M., van der Oost J. ( 2003). TRASH: a novel metal-binding domain predicted to be involved in heavy-metal sensing, trafficking and resistance. Trends Biochem Sci 28:170–173 [View Article][PubMed]
    [Google Scholar]
  17. Ettema T. J., Brinkman A. B., Lamers P. P., Kornet N. G., de Vos W. M., van der Oost J. ( 2006). Molecular characterization of a conserved archaeal copper resistance (cop) gene cluster and its copper-responsive regulator in Sulfolobus solfataricus P2. Microbiology 152:1969–1979 [View Article][PubMed]
    [Google Scholar]
  18. Felsenstein J. ( 1989). phylip – phylogeny inference package (version 3.2). Cladistics 5:164–166
    [Google Scholar]
  19. Fiala G., Stetter K. O. ( 1986). Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch Microbiol 145:56–61 [View Article]
    [Google Scholar]
  20. Gleissner M., Kaiser U., Antonopoulos E., Schäfer G. ( 1997). The archaeal SoxABCD complex is a proton pump in Sulfolobus acidocaldarius . J Biol Chem 272:8417–8426 [View Article][PubMed]
    [Google Scholar]
  21. Goldstein S., Meyerstein D., Czapski G. ( 1993). The Fenton reagents. Free Radic Biol Med 15:435–445 [View Article][PubMed]
    [Google Scholar]
  22. González-Guerrero M., Raimunda D., Cheng X., Argüello J. M. ( 2010). Distinct functional roles of homologous Cu+ efflux ATPases in Pseudomonas aeruginosa . Mol Microbiol 78:1246–1258 [View Article][PubMed]
    [Google Scholar]
  23. Grogan D. W. ( 1989). Phenotypic characterization of the archaebacterial genus Sulfolobus: comparison of five wild-type strains. J Bacteriol 171:6710–6719[PubMed]
    [Google Scholar]
  24. Haber F., Weiss J. ( 1932). Über die Katalyse des Hydroperoxydes. Naturwissenschaften 20:948–950 [View Article]
    [Google Scholar]
  25. Hassani B. K., Astier C., Nitschke W., Ouchane S. ( 2010). CtpA, a copper-translocating P-type ATPase involved in the biogenesis of multiple copper-requiring enzymes. J Biol Chem 285:19330–19337 [View Article][PubMed]
    [Google Scholar]
  26. Horng Y. C., Cobine P. A., Maxfield A. B., Carr H. S., Winge D. R. ( 2004). Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J Biol Chem 279:35334–35340 [View Article][PubMed]
    [Google Scholar]
  27. Imlay J. A. ( 2006). Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 59:1073–1082 [View Article][PubMed]
    [Google Scholar]
  28. Jonuscheit M., Martusewitsch E., Stedman K. M., Schleper C. ( 2003). A reporter gene system for the hyperthermophilic archaeon Sulfolobus solfataricus based on a selectable and integrative shuttle vector. Mol Microbiol 48:1241–1252 [View Article][PubMed]
    [Google Scholar]
  29. Kahn D., David M., Domergue O., Daveran M. L., Ghai J., Hirsch P. R., Batut J. ( 1989). Rhizobium meliloti fixGHI sequence predicts involvement of a specific cation pump in symbiotic nitrogen fixation. J Bacteriol 171:929–939[PubMed]
    [Google Scholar]
  30. Kaplan J. H. ( 2002). Biochemistry of Na,K-ATPase. Annu Rev Biochem 71:511–535 [View Article][PubMed]
    [Google Scholar]
  31. Koch H. G., Winterstein C., Saribas A. S., Alben J. O., Daldal F. ( 2000). Roles of the ccoGHIS gene products in the biogenesis of the cbb(3)-type cytochrome c oxidase. J Mol Biol 297:49–65 [View Article][PubMed]
    [Google Scholar]
  32. Komorowski L., Verheyen W., Schäfer G. ( 2002). The archaeal respiratory supercomplex SoxM from S. acidocaldarius combines features of quinole and cytochrome c oxidases. Biol Chem 383:1791–1799 [View Article][PubMed]
    [Google Scholar]
  33. Kroll J. S., Langford P. R., Wilks K. E., Keil A. D. ( 1995). Bacterial [Cu,Zn]-superoxide dismutase: phylogenetically distinct from the eukaryotic enzyme, and not so rare after all!. Microbiology 141:2271–2279 [View Article][PubMed]
    [Google Scholar]
  34. Kühlbrandt W. ( 2004). Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5:282–295 [View Article][PubMed]
    [Google Scholar]
  35. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. et al. ( 2007). clustal w and clustal_x version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  36. Lewinson O., Lee A. T., Rees D. C. ( 2009). A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc Natl Acad Sci U S A 106:4677–4682 [View Article][PubMed]
    [Google Scholar]
  37. Liochev S. I., Fridovich I. ( 2002). The Haber–Weiss cycle – 70 years later: an alternative view. Redox Rep 7:55–57, author reply 59–60 [View Article][PubMed]
    [Google Scholar]
  38. Lübben M., Kolmerer B., Saraste M. ( 1992). An archaebacterial terminal oxidase combines core structures of two mitochondrial respiratory complexes. EMBO J 11:805–812[PubMed]
    [Google Scholar]
  39. Lübben M., Arnaud S., Castresana J., Warne A., Albracht S. P., Saraste M. ( 1994). A second terminal oxidase in Sulfolobus acidocaldarius . Eur J Biochem 224:151–159 [View Article][PubMed]
    [Google Scholar]
  40. Møller J. V., Juul B., le Maire M. ( 1996). Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim Biophys Acta 1286:1–51[PubMed] [CrossRef]
    [Google Scholar]
  41. Nies D. H. ( 2003). Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339 [View Article][PubMed]
    [Google Scholar]
  42. Odermatt A., Suter H., Krapf R., Solioz M. ( 1993). Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae . J Biol Chem 268:12775–12779[PubMed]
    [Google Scholar]
  43. Osman D., Cavet J. S. ( 2008). Copper homeostasis in bacteria. Adv Appl Microbiol 65:217–247 [View Article][PubMed]
    [Google Scholar]
  44. Palmgren M. G., Axelsen K. B. ( 1998). Evolution of P-type ATPases. Biochim Biophys Acta 1365:37–45 [View Article][PubMed]
    [Google Scholar]
  45. Preisig O., Zufferey R., Hennecke H. ( 1996). The Bradyrhizobium japonicum fixGHIS genes are required for the formation of the high-affinity cbb3-type cytochrome oxidase. Arch Microbiol 165:297–305 [View Article][PubMed]
    [Google Scholar]
  46. Raimunda D., González-Guerrero M., Leeber B. W. III, Argüello J. M. ( 2011). The transport mechanism of bacterial Cu+-ATPases: distinct efflux rates adapted to different function. Biometals 24:467–475 [View Article][PubMed]
    [Google Scholar]
  47. Rensing C., Grass G. ( 2003). Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27:197–213 [View Article][PubMed]
    [Google Scholar]
  48. Rensing C., Fan B., Sharma R., Mitra B., Rosen B. P. ( 2000). CopA: An Escherichia coli Cu(I)-translocating P-type ATPase. Proc Natl Acad Sci U S A 97:652–656 [View Article][PubMed]
    [Google Scholar]
  49. Schelert J., Dixit V., Hoang V., Simbahan J., Drozda M., Blum P. ( 2004). Occurrence and characterization of mercury resistance in the hyperthermophilic archaeon Sulfolobus solfataricus by use of gene disruption. J Bacteriol 186:427–437 [View Article][PubMed]
    [Google Scholar]
  50. She Q., Singh R. K., Confalonieri F., Zivanovic Y., Allard G., Awayez M. J., Chan-Weiher C. C., Clausen I. G., Curtis B. A. et al. ( 2001). The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci U S A 98:7835–7840 [View Article][PubMed]
    [Google Scholar]
  51. Shungu D., Valiant M., Tutlane V., Weinberg E., Weissberger B., Koupal L., Gadebusch H., Stapley E. ( 1983). GELRITE as an Agar Substitute in Bacteriological Media. Appl Environ Microbiol 46:840–845[PubMed]
    [Google Scholar]
  52. Silver S., Phung L. T. ( 1996). Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–789 [View Article][PubMed]
    [Google Scholar]
  53. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. ( 1985). Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85 [View Article][PubMed]
    [Google Scholar]
  54. Solioz M., Vulpe C. ( 1996). CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci 21:237–241[PubMed] [CrossRef]
    [Google Scholar]
  55. Szabó Z., Sani M., Groeneveld M., Zolghadr B., Schelert J., Albers S. V., Blum P., Boekema E. J., Driessen A. J. ( 2007). Flagellar motility and structure in the hyperthermoacidophilic archaeon Sulfolobus solfataricus . J Bacteriol 189:4305–4309 [View Article][PubMed]
    [Google Scholar]
  56. Tottey S., Rich P. R., Rondet S. A., Robinson N. J. ( 2001). Two Menkes-type atpases supply copper for photosynthesis in Synechocystis PCC 6803. J Biol Chem 276:19999–20004 [View Article][PubMed]
    [Google Scholar]
  57. Villafane A. A., Voskoboynik Y., Cuebas M., Ruhl I., Bini E. ( 2009). Response to excess copper in the hyperthermophile Sulfolobus solfataricus strain 98/2. Biochem Biophys Res Commun 385:67–71 [View Article][PubMed]
    [Google Scholar]
  58. Villafane A., Voskoboynik Y., Ruhl I., Sannino D., Maezato Y., Blum P., Bini E. ( 2011). CopR of Sulfolobus solfataricus represents a novel class of archaeal-specific copper-responsive activators of transcription. Microbiology 157:2808–2817 [View Article][PubMed]
    [Google Scholar]
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