Terminal oxidase diversity and function in "Metallosphaera yellowstonensis": Gene expression and protein modeling suggest mechanisms of Fe(II) oxidation in the Sulfolobales

Applied and Environmental Microbiology

Volumn 77, Issue 5, 2011, Pages 1844-1853

  Kozubal, M A ^a   Dlakic M ^a   Macur, R E ^a   Inskeep, W P ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEON; BINDING DOMAIN; BLUE-COPPER PROTEINS; CYTOCHROME B; ELECTRON DONORS; GENE CLUSTERS; GENE SEQUENCES; GENOME SEQUENCES; HEME-COPPER OXIDASE; HETERODIMER COMPLEXES; IN-FIELD; METABOLIC PATHWAYS; METAGENOMES; MULTICOPPER OXIDASE; NICHE DIVERSIFICATION; OXIDIZING CONDITIONS; PLASTOCYANINS; PROTEIN COMPLEXES; PROTEIN MODELING; QUANTITATIVE PCR; REVERSE TRANSCRIPTASES; SULFITE OXIDASE; SULFUR OXIDATION; SUPERCOMPLEX; TERMINAL OXIDASE; TRACE METAL; YELLOWSTONE NATIONAL PARKS;

AMINO ACIDS; BIOLEACHING; COPPER; COPPER COMPOUNDS; OXIDATION; PARKS; POLYMERASE CHAIN REACTION; PORPHYRINS; PROTEINS; SULFUR; TRACE ELEMENTS;

GENE EXPRESSION;

FERROUS ION; OXIDOREDUCTASE; SULFUR;

AUTOTROPHY; CYTOCHROME; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; IRON; OXIDATION; PROTEIN; PYRITE; SULFUR; THERMOPHILY; TRACE METAL;

AEROBIC METABOLISM; ARTICLE; DNA SEQUENCE; ELECTRON TRANSPORT; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; METAGENOME; OXIDATION REDUCTION REACTION; SULFOLOBALES;

AEROBIOSIS; ELECTRON TRANSPORT; FERROUS COMPOUNDS; GENE EXPRESSION PROFILING; METABOLIC NETWORKS AND PATHWAYS; METAGENOME; OXIDATION-REDUCTION; OXIDOREDUCTASES; SEQUENCE ANALYSIS, DNA; SULFOLOBACEAE; SULFUR;

ARCHAEA; METALLOSPHAERA; SULFOLOBALES;

EID: 79953193433     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01646-10     Document Type: Article

References (63)

1. Amend, J. P., and E. L. Shock. 2001. Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25:175-243.
2. 3-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl. Environ. Microbiol. 65:4781-4787.
3. Arnold, K., L. Bordoli, J. Kopp, and T. Schwede. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modeling. Bioinformatics 22:195-201.
4. Auernik, K. S., Y. Maezato, P. H. Blum, and R. M. Kelly. 2008. The genome sequence of the metal-mobilizing, extremely thermoacidophilic archaeon Metallosphaera sedula provides insights into bioleaching-associated metabolism. Appl. Environ. Microbiol. 74:682-692.
5. Auernik, K. S., and R. M. Kelly. 2008. Identification of components of electron transport chains in the extremely thermoacidophilic crenarchaeon Metallosphaera sedula through iron and sulfur compound oxidation transcriptomes. Appl. Environ. Microbiol. 74:7723-7732.
6. Baker, B. J., and J. F. Banfield. 2003. Microbial communities in acid mine drainage. FEMS Microbiol. Ecol. 44:139-152.
7. Bandeiras, T. M., et al. 2009. The cytochrome ba complex from the thermoacidophilic crenarchaeote Acidianus ambivalens is an analog of bc(1) complexes. Biochim. Biophys. Acta 1787:37-45.
8. Bathe, S., and P. R. Norris. 2007. Ferrous iron- and sulfur-induced genes in Sulfolobus metallicus. Appl. Environ. Microbiol. 73:2491-2497.
9. Blake, R. C., E. A. Shute, J. Waskovsky, and A. P. Harrison, Jr. 1993. Respiratory components in acidophilic bacteria that respire on iron. Geomicrobiol. J. 10:173-192.
10. Blake, R., and D. B. Johnson. 2000. Phylogenetic and biochemical diversity among acidophilic bacteria that respire on iron, p. 53-78. In L. Derek (ed.), Environmental microbe-metal interactions. ASM Press, Washington, DC.
11. Brierley, C. L., and J. A. Brierley. 1973. A chemoautotrophic and thermophilic microorganism isolated from an acid hot spring. Can. J. Microbiol. 19:183-188.
12. Brock, T. D., K. M. Brock, R. T. Belly, and R. L. Weiss. 1972. Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch. Mikrobiol. 84:54-68.
13. Cowan, J. A. 1993. Inorganic biochemistry: an introduction. VCH Publishers, New York, NY.
14. Davis, A., et al. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35:W375-W383.
15. Dopson, M., C. Baker-Austin, and P. L. Bond. 2005. Analysis of differential protein expression during growth states of Ferroplasma strains and insights into electron transport for iron oxidation. Microbiology 151:4127-4137.
16. Fuchs, T., H. Huber, K. Teiner, S. Burggraf, and K. O. Stetter. 1995. Metallosphaera prunae, sp. nov., a novel metal-mobilizing, thermoacidophilic archaeum, isolated from a uranium mine in Germany. Syst. Appl. Microbiol. 18:560-566.
17. García-Horsman, J. A., B. Barquera, J. Rumbley, J. Ma, and R. B. Gennis. 1994. The superfamily of heme-copper respiratory oxidases. J. Bacteriol. 176:5587-5600.
18. Giri, A. V., S. Anishetty, and P. Gautam. 2004. Functionally specified protein signatures distinctive for each of the different blue copper proteins. BMC Bioinformatics 5:127.
19. Hallberg, K. B., and D. B. Johnson. 2001. Biodiversity of acidophilic prokaryotes. Adv. Appl. Microbiol. 49:37-84.
20. Hallmann, R., et al. 1993. Physiological characteristics of Thiobacillus ferrooxidans and Leptospirillum ferrooxidans and physiochemical factors influence microbial metal leaching. Geomicrobiol. J. 10:193-206.
21. Hedderich, R. 2004. Energy-converting [NiFe] hydrogenases from archaea and extremophiles: ancestors of complex I. J. Bioenerg. Biomembr. 36:65-75.
22. Hettmann, T., et al. 1998. Cytochrome b558/566 from the archaeon Sulfolobus acidocaldarius. A novel highly glycosylated, membrane-bound b-type hemoprotein. J. Biol. Chem. 273:12032-12040.
23. Huber, G., C. Spinnler, A. Gambacorta, and K. O. Stetter. 1989. Metallosphaera sedula gen. nov. and sp. nov. represents a new genus of aerobic, metal-mobilizing, thermoacidophilic archaebacteria. Syst. Appl. Microbiol. 12:38-47.
24. Huber, G., and K. O. Stetter. 1991. Sulfolobus metallicus, sp. nov., a novel strictly chemolithoautotrophic thermophilic archaeal species of metal-mobilizers. Syst. Appl. Microbiol. 14:372-378.
25. Inskeep, W. P., R. E. Macur, G. Harrison, B. C. Bostick, and S. Fendorf. 2004. Biomineralization of As(V)-hydrous ferric oxyhydroxide in microbial mats of an acid-sulfate-chloride geothermal spring, Yellowstone National Park. Geochim. Cosmochim. Acta 68:3141-3155.
26. Inskeep, W. P., et al. 2005. On the energetics of chemolithotrophy in nonequilibrium systems: case studies of geothermal springs in Yellowstone National Park. Geobiology 3:297-320.
27. Inskeep, W. P., et al. 2010. Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS One 5:e9773.
28. Johnson, D. B., and K. B. Hallberg. 2003. The microbiology of acidic mine waters. Res. Microbiol. 154:466-473.
29. Kappler, U., L. I. Sly, and A. G. McEwan. 2005. Respiratory gene clusters of Metallosphaera sedula: differential expression and transcriptional organization. Microbiology 151:35-43.
30. Kletzin, A., T. Urich, F. Müller, T. M. Bandeiras, and C. M. Gomes. 2004. Dissimilatory oxidation and reduction of elemental sulfur in thermophilic archaea. J. Bioenerg. Biomembr. 36:77-91.
31. Kloer, D. P., C. Hagel, J. Heider, and G. E. Schulz. 2006. Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14: 1377-1388.
32. Kniemeyer, O., and J. Heider. 2001. (S)-1-Phenylethanol dehydrogenase of Azoarcus sp. strain EbN1, an enzyme of anaerobic ethylbenzene catabolism. Arch. Microbiol. 176:129-135.
33. Komorowski, L., S. Anemüller, and G. Schäfer. 2001. First expression and characterization of a recombinant CuA-containing subunit II from an archaeal terminal oxidase complex. J. Bioenerg. Biomembr. 33:27-34.
34. Komorowski, L., and G. Schäfer. 2001. Sulfocyanin and subunit II, two copper proteins with novel features, provide new insight into the archaeal SoxM oxidase supercomplex. FEBS Lett. 487:351-355.
35. Komorowski, L., W. Verheyen, and G. Schäfer. 2002. The archaeal respiratory supercomplex SoxM from S. acidocaldarius combines features of quinole and cytochrome c oxidases. Biol. Chem. 383:1791-1799.
36. Kozubal, M., et al. 2008. Isolation and distribution of a novel iron-oxidizing crenarchaeon from acidic geothermal springs in Yellowstone National Park. Appl. Environ. Microbiol. 74:942-949.
37. Kurosawa, N., Y. H. Itoh, and T. Itoh. 2003. Reclassification of Sulfolobus hakonensis Takayanagi et al. 1996 as Metallosphaera hakonensis comb. nov. based on phylogenetic evidence and DNA G+C content. Int. J. Syst. Evol. Microbiol. 53:1607-1608.
38. Li, X., et al. 2007. Crystal structures of E. coli laccase CueO at different copper concentrations. Biochem. Biophys. Res. Commun. 354:21-26.
39. Lübben, M., B. Kolmerer, and M. Saraste. 1992. An archaebacterial terminal oxidase combines core structures of two mitochondrial respiratory complexes. EMBO J. 11:805-812.
40. Lübben, M., S. Warne, S. Albracht, and M. Saraste. 1994. The purified SoxABCD quinol oxidase complex of Sulfolobus acidocaldarius. Mol. Microbiol. 13:327-335.
41. Lübben, M., et al. 1994. A second terminal oxidase in Sulfolobus acidocaldarius. Eur. J. Biochem. 224:151-159.
42. Lüthy, R., J. U. Bowie, and D. Eisenberg. 1992. Assessment of protein models with three-dimensional profiles. Nature 356:83-85.
43. Macur, R. E., H. W. Langner, B. D. Kocar, and W. P. Inskeep. 2004. Linking geochemical processes with microbial community analysis: successional dynamics in an arsenic-rich, acid-sulfate-chloride geothermal spring. Geobiology 2:163-177.
44. Nakamura, K., and N. Go. 2005. Function and molecular evolution of multicopper blue proteins. Cell. Mol. Life Sci. 62:2050-2066.
45. Pereira, M. M., et al. 2004. Respiratory chains from aerobic thermophilic prokaryotes. J. Bioenerg. Biomembr. 36:93-105.
46. Poulos, T. L. 1996. The role of the proximal ligand in heme enzymes. J. Biol. Inorg. Chem. 1:356-359.
47. Purschke, W. G., C. L. Schmidt, A. Petersen, and G. Schäfer. 1997. The terminal quinol oxidase of the hyperthermophilic archaeon Acidianus ambivalens exhibits a novel subunit structure and gene organization. J. Bacteriol. 179:1344-1353.
48. Quintanar, L., M. Gebhard, T. P. Wang, D. J. Kosman, and E. I. Solomon. 2004. Ferrous binding to the multicopper oxidases Saccharomyces cerevisiae Fet3p and human ceruloplasmin: contributions to ferroxidase activity. J. Am. Chem. Soc. 126:6579-6589.
49. Rawlings, D. E. 2002. Heavy metal mining using microbes. Annu. Rev. Microbiol. 56:65-91.
50. Rawlings, D. E. 2005. Characteristics and adaptability of iron- and sulfuroxidizing microorganisms used for the recovery of metals from minerals and their concentrates. Microb. Cell Fact. 4:13.
51. Reno, M. L., N. L. Held, C. J. Fields, P. V. Burke, and R. J. Whitaker. 2009. Biogeography of the Sulfolobus islandicus pan-genome. Proc. Natl. Acad. Sci. U. S. A. 106:8605-8610.
52. Rohwerder, T., T. Gehrke, K. Kinzler, and W. Sand. 2003. Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl. Microbiol. Biotechnol. 63:239-248.
53. Singer, S. W., et al. 2008. Characterization of cytochrome 579, an unusual cytochrome isolated from an iron-oxidizing microbial community. Appl. Environ. Microbiol. 74:4454-4462.
54. Stoj, C. S., A. J. Augustine, L. Zeigler, E. I. Solomon, and D. J. Kosman. 2006. Structural basis of the ferrous iron specificity of the yeast ferroxidase, Fet3p. Biochemistry 45:12741-12749.
55. Suzuki, T., et al. 2002. Sulfolobus tokodaii sp. nov. (f. Sulfolobus sp. strain 7), a new member of the genus Sulfolobus isolated from Beppu Hot Springs, Japan. Extremophiles 6:39-44.
56. Takayanagi, S., et al. 1996. Sulfolobus hakonensis sp. nov., a novel species of acidothermophilic archaeon. Int. J. Syst. Bacteriol. 46:377-382.
57. To, T. B., D. K. Nordstrom, K. M. Cunningham, J. W. Ball, and R. B. McClesky. 1999. New method for the direct determination of dissolved Fe(III) concentration in acid mine waters. Environ. Sci. Technol. 33:807- 813.
58. van der Oost, J., et al. 1994. The heme-copper oxidase family consists of three distinct types of terminal oxidases and is related to nitric oxide reductase. FEMS Microbiol. Lett. 121:1-9.
59. Wallner, B., and A. Elofsson. 2003. Can correct protein models be identified? Protein Sci. 12:1073-1086.
60. Wiederstein, M., and M. J. Sippl. 2007. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 35:W407-W410.
61. Yarzábal, A., G. Brasseur, and V. Bonnefoy. 2002. Cytochromes c of Acidithiobacillus ferrooxidans. FEMS Microbiol. Lett. 209:189-195.
62. Yarzábal, A., et al. 2002. The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J. Bacteriol. 184:313-317.
63. Zähringer, U., H. Moll, T. Hettmann, Y. A. Knirel, and G. Schäfer. 2000. Cytochrome b558/566 from the archaeon Sulfolobus acidocaldarius has a unique Asn-linked highly branched hexasaccharide chain containing 6-sulfoquinovose. Eur. J. Biochem. 267:4144-4149.