1887

Abstract

The gene encoding a putative high-potential iron–sulfur protein (HiPIP) from the strictly acidophilic and chemolithoautotrophic ATCC 33020 has been cloned and sequenced. This potential HiPIP was overproduced in the periplasm of the neutrophile and heterotroph . As shown by optical and EPR spectra and by electrochemical studies, the recombinant protein has all the biochemical properties of a HiPIP, indicating that the iron–sulfur cluster was correctly inserted. Translocation of this protein in the periplasm of was not detected in a Δ mutant, indicating that it is dependent on the Tat system. The genetic organization of the locus in strains ATCC 23270 and ATCC 33020 is different from that found in strains Fe-1 and BRGM. Indeed, in ATCC 33020 and ATCC 23270 (the type strain), was not located downstream from but was instead downstream from , encoding cytochrome from the second cytochrome complex. These findings underline the genotypic heterogeneity within the species. The results suggest that Iro transfers electrons from a cytochrome complex to a terminal oxidase, as proposed for the HiPIP in photosynthetic bacteria.

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2005-05-01
2020-04-10
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References

  1. Agarwal A., Tan J., Eren M., Tevelev A., Lui S. M., Cowan J. A. 1993; Synthesis, cloning and expression of a synthetic gene for high potential iron protein from Chromatium vinosum. Biochem Biophys Res Commun197:1357–1362[CrossRef]
    [Google Scholar]
  2. Ambler R. P., Meyer T. E., Kamen M. D. 1993; Amino acid sequence of a high redox potential ferredoxin (HiPIP) from the purple phototrophic bacterium Rhodopila globiformis, which has the highest known redox potential of its class. Arch Biochem Biophys306:215–222[CrossRef]
    [Google Scholar]
  3. Appia-Ayme C. 1998; Caractérisation d'un opéron codant pour 7 protéines transporteurs d'électrons chez Thiobacillus ferrooxidans PhD thesis Université de la Méditerranée, Aix-Marseille II; France (in French):
    [Google Scholar]
  4. Appia-Ayme C., Bengrine A., Cavazza C., Giudici-Orticoni M.-T., Bruschi M., Chippaux M., Bonnefoy V. 1998; Characterization and expression of the co-transcribed cyc1 and cyc2 genes encoding the cytochrome c4 (c552) and a high-molecular-mass cytochromec from Thiobacillus ferrooxidans ATCC 33020. FEMS Microbiol Lett167:171–177
    [Google Scholar]
  5. Appia-Ayme C., Guiliani N., Ratouchniak J., Bonnefoy V. 1999; Characterization of an operon encoding two c-type cytochromes, an aa3-type cytochrome oxidase, and rusticyanin inThiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol65:4781–4787
    [Google Scholar]
  6. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. 1992; Current Protocols in Molecular Biology New York: Greene Publishing;
    [Google Scholar]
  7. Bartsch R. G. 1978; Purification of (4Fe-4S)1–2–ferredoxins (high-potential iron–sulfur proteins) from bacteria. Methods Enzymol53:329–340
    [Google Scholar]
  8. Bates R. G. 1964; Determination of pH New York: Wiley;
    [Google Scholar]
  9. Battaglia-Brunet F., Clarens M., d'Hugues P., Godon J.-J., Foucher S., Morin D. 2002; Monitoring of a pyrite-oxidising bacterial population using DNA single-strand conformation polymorphism and microscopic techniques. Appl Microbiol Biotechnol60:206–211[CrossRef]
    [Google Scholar]
  10. Bengrine A., Guiliani N., Appia-Ayme C., Jedlicki E., Holmes D. S., Chippaux M., Bonnefoy V. 1998; Sequence and expression of the rusticyanin structural gene from Thiobacillus ferrooxidans ATCC 33020 strain. Biochim Biophys Acta 1443;99–112[CrossRef]
    [Google Scholar]
  11. Berks B. C. 1996; A common export pathway for proteins binding complex redox cofactors?. Mol Microbiol22:393–404[CrossRef]
    [Google Scholar]
  12. Blake R. C., Shute E. A. II 1994; Respiratory enzymes of Thiobacillus ferrooxidans. Kinetic properties of an acid-stable iron : rusticyanin oxidoreductase. Biochemistry33:9220–9228[CrossRef]
    [Google Scholar]
  13. Blattner F. R., Plunkett G. III, Bloch C. A. 14 other authors 1997; The complete genome sequence of Escherichia coli K-12. Science277:1453–1474[CrossRef]
    [Google Scholar]
  14. Bonora P., Principi I., Monti B., Ciurli S., Zannoni D., Hochkoeppler A. 1999; On the role of high-potential iron-sulfur proteins and cytochromes in the respiratory chain of two facultative phototrophs. Biochim Biophys Acta 1410;51–60[CrossRef]
    [Google Scholar]
  15. Brasseur G., Bruscella P., Bonnefoy V., Lemesle-Meunier D. 2002; The bc1 complex of the iron-grown acidophilic chemolithotrophic bacterium Acidithiobacillus ferrooxidans functions in the reverse but not in the forward direction.Is there a second bc1 complex?. Biochim Biophys Acta1555:37–43[CrossRef]
    [Google Scholar]
  16. Brüser T., Deutzmann R., Dahl C. 1998; Evidence against the double-arginine motif as the only determinant for protein translocation by a novel Sec-independent pathway in Escherichia coli. FEMS Microbiol Lett164:329–336[CrossRef]
    [Google Scholar]
  17. Brüser T., Yano T., Brune D. C., Daldal F. 2003; Membrane targeting of a folded and cofactor-containing protein. Eur J Biochem270:1211–1221[CrossRef]
    [Google Scholar]
  18. Capozzi F., Ciurli S., Luchinat C. 1998; Coordination sphere versus protein environment as determinants of electronic and functional properties of iron-sulfur proteins. Struct Bonding90:127–160
    [Google Scholar]
  19. Carter C. W. Jr, Freer S. T., Nguyen-Huu-Xuong Alden, A R., Bartsch R. G, Kraut J.. 1974; Two-Angstrom crystal structure of oxidized Chromatium high potential iron protein. J Biol Chem249:4212–4225
    [Google Scholar]
  20. Casimiro D. R., Toy-Palmer A., Blake R. C., Dyson H. J. II 1995; Gene synthesis, high level expression, and mutagenesis of Thiobacillus ferrooxidans rusticyanin: His85 is a ligand to the blue copper center. Biochemistry34:6640–6648[CrossRef]
    [Google Scholar]
  21. Caspersen M. B., Bennett K., Christensen H. E. M. 2000; Expression and characterization of recombinant Rhodocyclus tenuis high potential iron-sulfur protein. Protein Expr Purif19:259–264[CrossRef]
    [Google Scholar]
  22. Cavazza C., Guigliarelli B., Bertrand P., Bruschi M. 1995; Biochemical and EPR characterization of a high potential iron-sulfur protein in Thiobacillus ferrooxidans. FEMS Microbiol Lett130:193–200[CrossRef]
    [Google Scholar]
  23. Collinet M.-N., Morin D. 1990; Characterization of arsenopyrite oxidizing Thiobacillus. Tolerance to arsenite, arsenate, ferrous and ferric iron. Antonie van Leeuwenhoek57:237–244[CrossRef]
    [Google Scholar]
  24. Cristobal S., de Gier J.-W., Nielsen H., von Heijne G. 1999; Competition between Sec- and Tat-dependent protein translocation in Escherichia coli. EMBO J18:2982–2990[CrossRef]
    [Google Scholar]
  25. Duquesne K., Lebrun S., Casiot C., Bruneel O., Personné J.-C., Leblanc M, Elbaz-Poulichet F., Morin G., Bonnefoy V. 2003; Immobilization of arsenite and ferric iron by Acidithiobacillus ferrooxidans and its relevance to acid mine drainage. Appl Environ Microbiol69:6165–6173[CrossRef]
    [Google Scholar]
  26. Elbehti A., Nitschke W., Tron P., Michel C., Lemesle-Meunier D. 1999; Redox components of cytochrome bc-type enzymes in acidophilic prokaryotes. I. Characterization of the cytochrome bc1-type complex of the acidophilic ferrous ion-oxidizing bacteriumThiobacillus ferrooxidans.. J Biol Chem274:16760–16765[CrossRef]
    [Google Scholar]
  27. Eltis L. D., Iwagami S. G., Smith M. 1994; Hyperexpression of a synthetic gene encoding a high potential iron sulfur protein. Protein Eng7:1145–1150[CrossRef]
    [Google Scholar]
  28. Fukumori Y., Yano T., Sato A., Yamanaka T. 1988; Fe(II)-oxidizing enzyme purified from Thiobacillus ferrooxidans. FEMS Microbiol Lett50:169–172[CrossRef]
    [Google Scholar]
  29. Furste J. P., Pansegrau W., Frank R., Blocker H., Scholz P., Bagdasarian M., Lanka E. 1986; Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene48:119–131[CrossRef]
    [Google Scholar]
  30. Giudici-Orticoni M.-T., Nitschke W., Cavazza C., Bruschi M. 1997; Characterization and functional role of a cytochrome c4 involved in the iron respiratory electron transport chain of Thiobacillus ferrooxidans. In Proceedings of the International Biohydrometallurgy Symposium IBS 97/Biomine 97PB4 1–PB4 10 Glenside, Australia: Australian Mineral Foundation;
    [Google Scholar]
  31. Giudici-Orticoni M.-T., Leroy G., Nitschke W., Bruschi M. 2000; Characterization of a new dihemic c4-type cytochrome isolated from Thiobacillus ferrooxidans. Biochemistry39:7205–7211[CrossRef]
    [Google Scholar]
  32. Goebel B. M., Stackebrandt E. 1994; Cultural and phylogenetic analysis of mixed microbial populations found in natural and commercial bioleaching environments. Appl Environ Microbiol60:1614–1621
    [Google Scholar]
  33. Guiliani N., Bengrine A., Borne F., Chippaux M., Bonnefoy V. 1995; Genetics of Thiobacillus ferrooxidans: advancement and projects: sequence and analysis of rus gene encoding rusticyanin and alaS gene encoding alanyl-tRNA synthetase. In Minerals Bioprocessing II pp95–110 Edited by Holmes D. S., Smith R. S.. Warrendale, PA: The Mineral, Metals and Material Society (TMS;
    [Google Scholar]
  34. Haladjian J., Bruschi M. Nunzi F., Bianco P. 1993; Electron-transfer reaction of rusticyanin, a “blue”-copper protein from Thiobacillus ferrooxidans, at modified gold electrodes. J Electroanal Chem352:329–335[CrossRef]
    [Google Scholar]
  35. Haladjian J., Bianco P., Nunzi F., Bruschi M. 1994; A permselective-membrane electrode for the electrochemical study of redox proteins. Application to cytochrome c552 from Thiobacillus ferrooxidans. Anal Chim Acta289:15–20[CrossRef]
    [Google Scholar]
  36. Harrison A. P. Jr. 1982; Genomic and physiological diversity amongst strains of Thiobacillus ferrooxidans, and genomic comparison with Thiobacillus thiooxidans. Arch Microbiol131:68–76[CrossRef]
    [Google Scholar]
  37. Harrison A. P. Jr. 1984; The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. Annu Rev Microbiol38:265–292[CrossRef]
    [Google Scholar]
  38. Heering H. A., Bulsink B. M., Hagen W. R., Meyer T. E. 1995; Influence of charge and polarity on the redox potentials of high-potential iron-sulfur proteins: evidence for the existence of two groups. Biochemistry34:14675–14686[CrossRef]
    [Google Scholar]
  39. Hochkoeppler A., Kofod P., Ferro G., Ciurli S. 1995; Isolation, characterization, and functional role of the high-potential iron-sulfur protein (HiPIP) from Rhodoferax fermentans.. Arch Biochem Biophys322:313–318[CrossRef]
    [Google Scholar]
  40. Hochkoeppler A., Zannoni D., Ciurli S., Meyer T. E., Cusanovich M. A., Tollin G. 1996; Kinetics of photo-induced electron transfer from high-potential iron-sulfur protein to the photosynthetic reaction center of the purple phototroph Rhodoferax fermentans. Proc Natl Acad Sci U S A93:6998–7002[CrossRef]
    [Google Scholar]
  41. Ingledew W. J. 1982; Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta683:89–117[CrossRef]
    [Google Scholar]
  42. Irazabal N., Amils R, Marín I.. 1997; Genomic organization of the acidophilic chemolithoautotrophic bacterium Thiobacillus ferrooxidans ATCC 21834. J Bacteriol179:1946–1950
    [Google Scholar]
  43. Kai M., Yano T., Tamegai H., Fukumori Y., Yamanaka T. 1992; Thiobacillus ferrooxidans cytochrome c oxidase: purification, and molecular and enzymatic features. J Biochem112:816–821
    [Google Scholar]
  44. Karavaiko G. I., Turova T. P., Kondrat'eva T. F., Lysenko A. M., Kolganova T. V., Ageeva S. N., Muntyan L. N., Pivovarova T. A. 2003; Phylogenetic heterogeneity of the species Acidithiobacillus ferrooxidans. Int J Syst Evol Microbiol53:113–119[CrossRef]
    [Google Scholar]
  45. Kelly D. P., Wood A. P. 2000; Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen.nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol50:511–516[CrossRef]
    [Google Scholar]
  46. Kusano T., Takeshima T., Sugarawa K., Inoue C., Shiratori T., Yano T., Fukumori Y., Yamanaka T. 1992; Molecular cloning of the gene encoding Thiobacillus ferrooxidans Fe(II) oxidase. High homology of the gene product with HiPIP. J Biol Chem267:11242–11247
    [Google Scholar]
  47. Leduc L. G., Ferroni G. D. 1994; The chemolithotrophic bacterium Thiobacillus ferrooxidans. FEMS Microbiol Lett14:103–120[CrossRef]
    [Google Scholar]
  48. Liu Z., Guiliani N., Appia-Ayme C., Borne F., Ratouchniak J., Bonnefoy V. 2000; Construction and characterization of a recA mutant of Thiobacillus ferrooxidans by marker exchange mutagenesis. J Bacteriol182:2269–2276[CrossRef]
    [Google Scholar]
  49. Lovenberg W., Buchanan B. B., Rabinowitz J. C. 1963; Studies on the chemical nature of clostridial ferredoxin. J Biol Chem238:3899–3913
    [Google Scholar]
  50. Menin L., Schoepp B., Parot P., Verméglio A. 1997; Photoinduced cyclic electron transfer in Rhodocyclus tenuis cells: participation of HiPIP or cyt c8 depending on the ambient redox potential. Biochemistry36:12183–12188[CrossRef]
    [Google Scholar]
  51. Nagashima K. V., Matsuura K., Shimada K., Verméglio A. 2002; High-potential iron-sulfur protein (HiPIP) is the major electron donor to the reaction center complex in photosynthetically growing cells of the purple bacterium Rubrivivax gelatinosus. Biochemistry41:14028–14032[CrossRef]
    [Google Scholar]
  52. Novo M. T. M., de Souza A. P., Garcia O., Ottoboni L. M. M. 1996; RAPD genomic fingerprinting differentiates Thiobacillus ferrooxidans strains. Syst Appl Microbiol19:91–95[CrossRef]
    [Google Scholar]
  53. Ochman H., Medhora M. M., Garza D., Hartl D. L. 1990; Amplification of flanking sequences by inverse PCR. In PCR Protocols, a Guide to Methods and Applications pp219–227 Edited by Innis M. A., Gelfand D. H., Sninsky J. J., White T. J.. San Diego: Academic Press;
    [Google Scholar]
  54. Palmer T., Berks B. C. 2003; Moving folded proteins across the bacterial cell membrane. Microbiology149:547–556[CrossRef]
    [Google Scholar]
  55. Pereira M. M., Carita J. N., Teixeira M. 1999; Membrane-bound electron transfer chain of the thermohalophilic bacterium Rhodothermus marinus: characterization of the iron-sulfur centers from the dehydrogenases and investigation of the high-potential iron-sulfur protein function by in vitro reconstitution of the respiratory chain. Biochemistry38:1276–1283[CrossRef]
    [Google Scholar]
  56. Schoepp B., Parot P., Menin L., Gaillard J., Richaud P, Verméglio A. 1995; In vivo participation of a high potential iron-sulfur protein as electron donor to the photochemical reaction center ofRubrivivax gelatinosus. Biochemistry34:11736–11742[CrossRef]
    [Google Scholar]
  57. Selenska-Pobell S., Otto A., Kutschke S. 1998; Identification and discrimination of thiobacilli using ARDREA, RAPD and rep-APD. J Appl Microbiol84:1085–1091[CrossRef]
    [Google Scholar]
  58. Takahashi Y., Nakamura M. 1999; Functional assignment of the ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster involved in the assembly of Fe-S clusters inEscherichia coli. J Biochem126:917–926[CrossRef]
    [Google Scholar]
  59. Takahashi Y., Tokumoto U. 2002; A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J Biol Chem277:28380–28383[CrossRef]
    [Google Scholar]
  60. Tedro S. M., Meyer T. E., Kamen M. D. 1979; Primary structure of a high potential, four-iron-sulfur ferredoxin from the photosynthetic bacterium Rhodospirillum tenue. J Biol Chem254:1495–1500
    [Google Scholar]
  61. Tedro S. M., Meyer T. E., Kamen M. D. 1985; The amino acid sequence of a high-redox-potential ferredoxin from the purple phototrophic bacterium, Rhodospirillum tenue strain 2761. Arch Biochem Biophys239:94–101[CrossRef]
    [Google Scholar]
  62. Valdés J., Veloso F., Jedlicki E., Holmes D. 2003; Metabolic reconstruction of sulfur assimilation in the extremophile Acidithiobacillus ferrooxidans based on genome analysis. BMC Genomics4:51 doi:10.1186/1471-2164-4-51[CrossRef]
    [Google Scholar]
  63. Van Driessche G., Vandenberghe I., Devreese B.. 7 other authors 2003; Amino acid sequences and distribution of high-potential iron-sulfur proteins that donate electrons to the photosynthetic reaction center in phototropic proteobacteria. J Mol Evol57:181–199[CrossRef]
    [Google Scholar]
  64. Verméglio A., Li J., Schoepp-Cothenet B., Pratt N., Knaff D. B. 2002; The role of high-potential iron protein and cytochrome c8 as alternative electron donors to the reaction center ofChromatium vinosum. Biochemistry41:8868–8875[CrossRef]
    [Google Scholar]
  65. Wu L.-F., Ize B., Chanal A., Quentin Y., Fichant G. 2000; Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J Mol Microbiol Biotechnol2:179–189
    [Google Scholar]
  66. Yamanaka T., Fukumori Y. 1995; Molecular aspects of the electron transfer system which participates in the oxidation of ferrous ion by Thiobacillus ferrooxidans. FEMS Microbiol Lett17:401–413[CrossRef]
    [Google Scholar]
  67. Yarzábal A., Brasseur G., Ratouchniak J., Lund K., Lemesle-Meunier D., DeMoss J. A., Bonnefoy V. 2002; The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol184:313–317[CrossRef]
    [Google Scholar]
  68. Yarzábal A., Appia-Ayme C., Ratouchniak J., Bonnefoy V. 2004; Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology150:2113–2123[CrossRef]
    [Google Scholar]
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