A systems view of haloarchaeal strategies to withstand stress from transition metals

Genome Research

Volumn 16, Issue 7, 2006, Pages 841-854

  Kaur, Amardeep ^a   Pan, Min ^a   Meislin, Megan ^a   Facciotti, Marc T ^a   El Gewely, Raafat ^b   Baliga, Nitin S ^a  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

COBALT; CUPRIC ION; FERRITIN; FERROUS ION; MANGANESE; METAL; NICKEL; REACTIVE OXYGEN METABOLITE; TRANSITION ELEMENT; ZINC;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CELL FUNCTION; CHELATION; HALOBACTERIUM; HALOPHILIC BACTERIUM; ION TRANSPORT; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; STEADY STATE; STRESS; SYNTHESIS; TRANSCRIPTION INITIATION; UPREGULATION;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HALOBACTERIUM; METALS, HEAVY; MODELS, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSITION ELEMENTS;

ARCHAEA; HALOBACTERIUM;

EID: 33745619803     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.5189606     Document Type: Article

References (82)

1. Alekshun, M.N., Levy, S.B., Mealy, T.R., Seaton, B.A., and Head, J.F. 2001. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 Å resolution. Nat. Struct. Biol. 8: 710-714.
2. Andrews, N.C. 2002. Metal transporters and disease. Curr. Opin. Chem. Biol. 6: 181-186.
3. Babich, H. and Stotzky, G. 1980. Environmental factors that influence the toxicity of heavy metal and gaseous pollutants to microorganisms. Crit. Rev. Microbiol. 8: 99-145.
4. Baichoo, N., Wang, T., Ye, R., and Helmann, J.D. 2002. Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol. Microbiol. 45: 1613-1629.
5. Baliga, N.S., Goo, Y.A., Ng, W.V., Hood, L., Daniels, C.J., and DasSarma, S. 2000. Is gene expression in Halobacterium NRC-1 regulated by multiple TBP and TFB transcription factors? Mol. Microbiol. 36: 1184-1185.
6. Baliga, N.S., Pan, M., Goo, Y.A., Yi, E.C., Goodlett, D.R., Dimitrov, K., Shannon, P., Aebersold, R., Ng, W.V., and Hood, L. 2002. Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach. Proc. Natl. Acad. Sci. 99: 14913-14918.
7. Baliga, N.S., Bjork, S.J., Bonneau, R., Pan, M., Iloanusi, C., Kottemann, M.C.H., Hood, L., and DiRuggiero, J. 2004. Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC-1. Genome Res. 14: 1025-1035.
8. Bateman, A., Birney, E., Durbin, R., Eddy, S.R., Howe, K.L., and Sonnhammer, E.L. 2000. The Pfam protein families database. Nucleic Acids Res. 28: 263-266.
9. Blindauer, C.A., Harrison, M.D., Robinson, A.K., Parkinson, J.A., Bowness, P.W., Sadler, P.J., and Robinson, N.J. 2002. Multiple bacteria encode metallothioneins and SmtA-like zinc fingers. Mol. Microbiol. 45: 1421-1432.
10. Bonneau, R., Baliga, N.S., Deutsch, E.W., Shannon, P., and Hood, L. 2004. Comprehensive de novo structure prediction in a systems-biology context for the archaea Halobacterium sp. NRC-1. Genome Biol. 5: R52.
11. Bonneau, R., Reiss, D.J., Shannon, P., Facciotti, M., Hood, L., Baliga, N.S., and Thorsson, V. 2006. The Inferelator: An algorithm for learning parsimonious regulatory networks from systems-biology data sets de novo. Genome Biol. 7: R36.
12. Cavet, J.S., Meng, W., Pennella, M.A., Appelhoff, R.J., Giedroc, D.P., and Robinson, N.J. 2002. A nickel-cobalt-sensing ArsR-SmtB family repressor. Contributions of cytosol and effector binding sites to metal selectivity. J. Biol. Chem. 277: 38441-38448.
13. Chimienti, F., Jourdan, E., Favier, A., and Seve, M. 2001. Zinc resistance impairs sensitivity to oxidative stress in HeLa cells: Protection through metallothioneins expression. Free Radic. Biol. Med. 31: 1179-1190.
14. Cook, W.J., Kar, S.R., Taylor, K.B., and Hall, L.M. 1998. Crystal structure of the cyanobacterial metallothionein repressor SmtB: A model for metalloregulatory proteins. J. Mol. Biol. 275: 337-346.
15. Degtyarenko, K. 2000. Bioinorganic motifs: Towards functional classification of metalloproteins. Bioinformatics 16: 851-864.
16. Ercal, N., Gurer-Orhan, H., and Aykin-Burns, N. 2001. Toxic metals and oxidative stress part I: Mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 1: 529-539.
17. Ettema, T.J., Huynen, M.A., de Vos, W.M., and 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.
18. Facciotti, M.T., Bonneau, R., Hood, L., and Baliga, N.S. 2004. Systems biology experimental design - considerations for building predictive gene regulatory network models for prokaryotic systems. Curr. Genomics 5: 527-544.
19. Fellenberg, K., Hauser, N.C., Brors, B., Neutzner, A., Hoheisel, J.D., and Vingron, M. 2001. Correspondence analysis applied to microarray data. Proc. Natl. Acad. Sci. 98: 10781-10786.
20. Finney, L.A. and O'Halloran, T.V. 2003. Transition metal speciation in the cell: Insights from the chemistry of metal ion receptors. Science 300: 931-936.
21. Forbes, J.R., Hsi, G., and Cox, D.W. 1999. Role of the copper-binding domain in the copper transport function of ATP7B, the P-type ATPase defective in Wilson disease. J. Biol. Chem. 274: 12408-12413.
22. Gavella, M., Lipovac, V., Vucic, M., and Sverko, V. 1999. In vitro inhibition of superoxide anion production and superoxide dismutase activity by zinc in human spermatozoa. Int. J. Androl. 22: 266-274.
23. Grass, G. and Rensing, C. 2001. Genes involved in copper homeostasis in Escherichia coli. J. Bacteriol. 183: 2145-2147.
24. Guedon, E., Moore, C.M., Que, Q., Wang, T., Ye, R.W., and Helmann, J.D. 2003. The global transcriptional response of Bacillus subtilis to manganese involves the MntR, Fur, TnrA and σB regulons. Mol. Microbiol. 49: 1477-1491.
25. Haber, F. and Weiss, J. 1934. The catalytic decomposition of hydrogen peroxide by iron salts. Proc. R. Soc. London, Ser. A. 147: 332-351.
26. Hamza, I., Schaefer, M., Klomp, L.W., and Gitlin, J.D. 1999. Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis. Proc. Natl. Acad. Sci. 96: 13363-13368.
27. Hantke, K. 2001. Iron and metal regulation in bacteria. Curr. Opin. Microbiol. 4: 172-177.
28. Hou, Z. and Mitra, B. 2003. The metal specificity and selectivity of ZntA from Escherichia coli using the acylphosphate intermediate. J. Biol. Chem. 278: 28455-28461.
29. Hung, I.H., Casareno, R.L., Labesse, G., Mathews, F.S., and Gitlin, J.D. 1998. HAH1 is a copper-binding protein with distinct amino acid residues mediating copper homeostasis and antioxidant defense. J. Biol. Chem. 273: 1749-1754.
30. Ideker, T., Thorsson, V., Siegel, A.F., and Hood, L.E. 2000. Testing for differentially-expressed genes by maximum-likelihood analysis of microarray data. J. Comput. Biol. 7: 805-817.
31. Ideker, T., Thorsson, V., Ranish, J.A., Christmas, R., Buhler, J., Eng, J.K., Bumgarner, R., Goodlett, D.R., Aebersold, R., and Hood, L. 2001. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292: 929-934.
32. Jakubovics, N.S. and Jenkinson, H.F. 2001. Out of the iron age: New insights into the critical role of manganese homeostasis in bacteria. Microbiol. 147: 1709-1718.
33. Jensen, L.T., Ajua-Alemanji, M., and Culotta, V.C. 2003. The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis. J. Biol. Chem. 278: 42036-42040.
34. Jordan, I.K., Natale, D.A., Koonin, E.V., and Galperin, M.Y. 2001. Independent evolution of heavy metal-associated domains in copper chaperones and copper-transporting atpases. J. Mol. Evol. 53: 622-633.
35. Kanehisa, M. 2002. The KEGG database. Novartis Found. Symp. 247: 91-101; discussion 101-103, 119-128, 244-252.
36. Kehrer, J.P. 2000. The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149: 43-50.
37. Kennedy, S.P., Ng, W.V., Salzberg, S.L., Hood, L., and DasSarma, S. 2001. Understanding the adaptation of Halobacterium species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res. 11: 1641-1650.
38. Kirschner, M.W. 2005. The meaning of systems biology. Cell 121: 503-504.
39. Larin, D., Mekios, C., Das, K., Ross, B., Yang, A.S., and Gilliam, T.C. 1999. Characterization of the interaction between the Wilson and Menkes disease proteins and the cytoplasmic copper chaperone, HAH1p. J. Biol. Chem. 274: 28497-28504.
40. Lin, S.J., Pufahl, R.A., Dancis, A., O'Halloran, T.V., and Culotta, V.C. 1997. A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J. Biol. Chem. 272: 9215-9220.
41. Medicis, E.D., Paquette, J., Gauthier, J.J., and Shapcott, D. 1986. Magnesium and manganese content of halophilic bacteria. Appl. Environ. Microbiol. 52: 567-573.
42. Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7: 405-410.
43. Moore, C.M., Gaballa, A., Hui, M., Ye, R.W., and Helmann, J.D. 2005. Genetic and physiological responses of Bacillus subtilis to metal ion stress. Mol. Microbiol. 57: 27-40.
44. Moreno-Hagelsieb, G. and Collado-Vides, J. 2002. A powerful non-homology method for the prediction of operons in prokaryotes. Bioinformatics (Suppl 1) 18: S329-S336.
45. Munro, H.N. and Linder, M.C. 1978. Ferritin: Structure, biosynthesis, and role in iron metabolism. Physiol. Rev. 58: 317-396.
46. Nair, S. and Finkel, S.E. 2004. Dps protects cells against multiple stresses during stationary phase. J. Bacteriol. 186: 4192-4198.
47. Nelson, N. 1999. Metal ion transporters and homeostasis. EMBO J. 18: 4361-4371.
48. Ng, W.V., Kennedy, S.P., Mahairas, G.G., Berquist, B., Pan, M., Shukla, H.D., Lasky, S.R., Baliga, N.S., Thorsson, V., Sbrogna, J., et al. 2000. From the cover: Genome sequence of Halobacterium species NRC-1. Proc. Natl. Acad. Sci. 97: 12176-12181.
49. Nieto, J.J., Fernandez-Castillo, R., Marquez, M.C., Ventosa, A., Quesada, E., and Ruiz-Berraquero, F. 1989. Survey of metal tolerance in moderately halophilic eubacteria. Appl. Environ. Microbiol. 55: 2385-2390.
50. O'Halloran, T.V. 1993. Transition metals in control of gene expression. Science 261: 715-725.
51. Outten, C.E. and O'Halloran, T.V. 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292: 2488-2492.
52. Overbeek, R., Fonstein, M., D'Souza, M., Pusch, G.D., and Maltsev, N. 1999. The use of gene clusters to infer functional coupling. Proc. Natl. Acad. Sci. 96: 2896-2901.
53. Patzer, S.I. and Hantke, K. 1998. The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol. Microbiol. 28: 1199-1210.
54. Pellegrini, M., Marcotte, E.M., Thompson, M.J., Eisenberg, D., and Yeates, T.O. 1999. Assigning protein functions by comparative genome analysis: Protein phylogenetic profiles. Proc. Natl. Acad. Sci. 96: 4285-4288.
55. Que, Q. and Helmann, J.D. 2000. Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins. Mol. Microbiol. 35: 1454-1468.
56. Raab, A. and Feldmann, J. 2003. Microbial transformation of metals and metalloids. Sci. Prog. 86: 179-202.
57. Reindel, S., Anemuller, S., Sawaryn, A., and Matzanke, B.F. 2002. The DpsA-homologue of the archaeon Halobacterium salinarum is a ferritin. Biochim. Biophys. Acta 1598: 140-146.
58. Reindel, S., Schmidt, C.L., Anemuller, S., and Matzanke, B.F. 2005. Expression and regulation pattern of ferritin-like DpsA in the archaeon Halobacterium Salinarum. Biometals 18: 387-397.
59. Rensing, C., Mitra, B., and Rosen, B.P. 1997. The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc. Natl. Acad. Sci. 94: 14326-14331.
60. Rensing, C., Sun, Y., Mitra, B., and Rosen, B.P. 1998. Pb(II)-translocating P-type ATPases. J. Biol. Chem. 273: 32614-32617.
61. Rensing, C., Ghosh, M., and Rosen, B.P. 1999. Families of soft-metal-ion-transporting ATPases. J. Bacteriol. 181: 5891-5897.
62. Schelert, J., Dixit, V., Hoang, V., Simbahan, J., Drozda, M., and 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.
63. Shannon, P.T., Reiss, D.J., Bonneau, R., and Baliga, N.S. 2006. Gaggle: An open-source software system for integrating bioinformatics software and data sources. BMC Bioinformatics 7: 176.
64. Sharma, R., Rensing, C., Rosen, B.P., and Mitra, B. 2000. The ATP hydrolytic activity of purified ZntA, a Pb(II)/Cd(II)/Zn(II)-translocating ATPase from Escherichia coli. J. Biol. Chem. 275: 3873-3878.
65. Silver, S. 1992. Plasmid-determined metal resistance mechanisms: Range and overview. Plasmid 27: 1-3.
66. Strausak, D., Mercer, J.F., Dieter, H.H., Stremmel, W., and Multhaup, G. 2001. Copper in disorders with neurological symptoms: Alzheimer's, Menkes, and Wilson diseases. Brain Res. Bull. 55: 175-185.
67. Sunkar, R., Bartels, D., and Kirch, H.H. 2003. Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J. 35: 452-464.
68. Sussman, J.L., Lin, D., Jiang, J., Manning, N.O., Prilusky, J., Ritter, O., and Abola, E.E. 1998. Protein Data Bank (PDB): Database of three-dimensional structural information of biological macromolecules. Acta Crystallogr. D Biol. Crystallogr. 54: 1078-1084.
69. Takeyama, Y., Ogino, K., Segawa, H., Kobayashi, H., Uda, T., and Houbara, T. 1995. Effects of zinc on production of active oxygen species by rat neutrophils. Pharmacol. Toxicol. 76: 50-55.
70. Tatusov, R.L., Galperin, M.Y., Natale, D.A., and Koonin, E.V. 2000. The COG database: A tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28: 33-36.
71. Theil, E.C. 1987. Ferritin: Structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu. Rev. Biochem. 56: 289-315.
72. 2+ to discriminate endonucleases activated during apoptosis. Biochimie 79: 435-438.
73. Tottey, S., Rondet, S.A., Borrelly, G.P., Robinson, P.J., Rich, P.R., and Robinson, N.J. 2002. A copper metallochaperone for photosynthesis and respiration reveals metal-specific targets, interaction with an importer, and alternative sites for copper acquisition. J. Biol. Chem. 277: 5490-5497.
74. Tottey, S., Harvie, D.R., and Robinson, N.J. 2005. Understanding how cells allocate metals using metal sensors and metallochaperones. Acc. Chem. Res. 38: 775-783.
75. Tusher, V.G., Tibshirani, R., and Chu, G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. 98: 5116-5121.
76. Valko, M., Morris, H., and Cronin, M.T. 2005. Metals, toxicity and oxidative stress. Curr. Med. Chem. 12: 1161-1208.
77. Wang, G., Kennedy, S.P., Fasiludeen, S., Rensing, C., and DasSarma, S. 2004. Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. J. Bacteriol. 186: 3187-3194.
78. Weston, A.D., Baliga, N.S., Bonneau, R., and Hood, L. 2003. Systems approaches applied to the study of Saccharomyces cerevisiae and Halobacterium sp. Cold Spring Harb. Symp. Quant. Biol. 68: 345-357.
79. Wiedenheft, B., Mosolf, J., Willits, D., Yeager, M., Dryden, K.A., Young, M., and Douglas, T. 2005. An archaeal antioxidant: Characterization of a Dps-like protein from Sulfolobus solfataricus. Proc. Natl. Acad. Sci. 102: 10551-10556.
80. Winkelmann, G. 2002. Microbial siderophore-mediated transport. Biochem. Soc. Trans. 30: 691-696.
81. Winterbourn, C.C. 1995. Toxicity of iron and hydrogen peroxide: The Fenton reaction. Toxicol. Lett. 82-83: 969-974.
82. Zeth, K., Offermann, S., Essen, L.O., and Oesterhelt, D. 2004. Iron-oxo clusters biomineralizing on protein surfaces: Structural analysis of Halobacterium salinarum DpsA in its low- and high-iron states. Proc. Natl. Acad. Sci. 101: 13780-13785.