The HiPIP from the acidophilic Acidithiobacillus ferrooxidans is correctly processed and translocated in Escherichia coli, in spite of the periplasm pH difference between these two micro-organisms

Microbiology

Volumn 151, Issue 5, 2005, Pages 1421-1431

  Bruscella, Patrice ^a   Cassagnaud, Laure ^a   Ratouchniak, Jeanine ^a   Brasseur, Gaël ^b   Lojou, Elisabeth ^b   Amils, Ricardo ^c   Bonnefoy, Violaine ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C1; IRON SULFUR PROTEIN; OXIDOREDUCTASE; RECOMBINANT PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE;

ACIDITHIOBACILLUS FERROOXIDANS; ARTICLE; BACTERIAL STRAIN; BACTERIAL TRANSLOCATION; CELL PH; CHEMICAL ANALYSIS; CLUSTER ANALYSIS; CONTROLLED STUDY; CYTOPLASM; DOWNSTREAM PROCESSING; ELECTROCHEMICAL ANALYSIS; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ESCHERICHIA COLI; GENE LOCUS; GENETIC CODE; GENETIC HETEROGENEITY; GENETIC ORGANIZATION; HETEROTROPHY; MICROORGANISM; MOLECULAR CLONING; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN TRANSPORT; SEQUENCE ANALYSIS; SPECIES DIFFERENCE;

ACIDITHIOBACILLUS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLONING, MOLECULAR; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; IRON-SULFUR PROTEINS; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PERIPLASM; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; SEQUENCE ANALYSIS, DNA;

ACIDITHIOBACILLUS FERROOXIDANS; ESCHERICHIA COLI; PHOTOBACTERIA;

EID: 19044374613     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27476-0     Document Type: Article

References (68)

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 Commun 197, 1357-1362.
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 Biophys 306, 215-222.
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).
4. 552) and a high-molecular-mass cytochrome c from Thiobacillus ferrooxidans ATCC 33020. FEMS Microbiol Lett 167, 171-177.
5. 3-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65, 4781-4787.
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.
7. Bartsch, R. G. (1978). Purification of (4Fe-4S)1-2-ferredoxins (high-potential iron-sulfur proteins) from bacteria. Methods Enzymol 53, 329-340.
8. Bates, R. G. (1964). Determination of pH. New York: Wiley.
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 Biotechnol 60, 206-211.
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.
11. Berks, B. C. (1996). A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22, 393-404.
12. Blake, R. C., II & Shute, E. A. (1994). Respiratory enzymes of Thiobacillus ferrooxidans. Kinetic properties of an acid-stable iron : rusticyanin oxidoreductase. Biochemistry 33, 9220-9228.
13. Blattner, F. R., Plunkett, G., III, Bloch, C. A. & 14 other authors (1997). The complete genome sequence of Escherichia coli K-12. Science 277, 1453-1474.
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.
15. 1 complex? Biochim Biophys Acta 1555, 37-43.
16. Brüser, T., Deutzmann, R. & Dahl, C. (1998). Evidence against the double-arginine motif as the only determinant for protein translocation by a novel See-independent pathway in Escherichia coli. FEMS Microbiol Lett 164, 329-336.
17. Brüser, T., Yano, T., Brune, D. C. & Daldal, F. (2003). Membrane targeting of a folded and cofactor-containing protein. Eur J Biochem 270, 1211-1221.
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 Bonding 90, 127-160.
19. Carter, C. W., Jr, Kraut, J., Freer, S. T., Nguyen-Huu-Xuong, Alden, R. A. & Bartsch, R. G. (1974). Two-Angstrom crystal structure of oxidized Chromatium high potential iron protein. J Biol Chem 249, 4212-4225.
20. Casimiro, D. R., Toy-Palmer, A., Blake, R. C., II & Dyson, H. J. (1995). Gene synthesis, high level expression, and mutagenesis of Thiobacillus ferrooxidans rusticyanin: His85 is a ligand to the blue copper center. Biochemistry 34, 6640-6648.
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 Purif 19, 259-264.
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 Lett 130, 193-200.
23. Collinet, M.-N. & Morin, D. (1990). Characterization of arsenopyrite oxidizing Thiobacillus. Tolerance to arsenite, arsenate, ferrous and ferric iron. Antonie van Leeuwenhoek 57, 237-244.
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 J 18, 2982-2990.
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 Microbiol 69, 6165-6173.
26. 1-type complex of the acidophilic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans. J Biol Chem 274, 16760-16765.
27. Eltis, L. D., Iwagami, S. G. & Smith, M. (1994). Hyperexpression of a synthetic gene encoding a high potential iron sulfur protein. Protein Eng 7, 1145-1150.
28. Fukumori, Y., Yano, T., Sato, A. & Yamanaka, T. (1988). Fe(II)-oxidizing enzyme purified from Thiobacillus ferrooxidans. FEMS Microbiol Lett 50, 169-172.
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. Gene 48, 119-131.
30. 4 involved in the iron respiratory electron transport chain of Thiobacillus ferrooxidans. In Proceedings of the International Biohydrometallurgy Symposium IBS 97 /Biomine 97, PB4 1-PB4 10. Glenside, Australia: Australian Mineral Foundation.
31. 4-type cytochrome isolated from Thiobacillus ferrooxidans. Biochemistry 39, 7205-7211.
32. Goebel, B. M. & Stackebrandt, E. (1994). Cultural and phylogenetic analysis of mixed microbial populations found in natural and commercial bioleaching environments. Appl Environ Microbiol 60, 1614-1621.
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, pp. 95-110. Edited by D. S. Holmes & R. S. Smith. Warrendale, PA: The Mineral, Metals and Material Society (TMS).
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 Chem 352, 329-335.
35. 552 from Thiobacillus ferrooxidans. Anal Chim Acta 289, 15-20.
36. Harrison, A. P., Jr (1982). Genomic and physiological diversity amongst strains of Thiobacillus ferrooxidans, and genomic comparison with Thiobacillus thiooxidans. Arch Microbiol 131, 68-76.
37. Harrison, A. P., Jr (1984). The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. Annu Rev Microbiol 38, 265-292.
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. Biochemistry 34, 14675-14686.
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 Biophys 322, 313-318.
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 A 93, 6998-7002.
41. Ingledew, W. J. (1982). Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta 683, 89-117.
42. Irazabal, N., Marín, I. & Amils, R. (1997). Genomic organization of the acidophilic chemolithoautotrophic bacterium Thiobacillus ferrooxidans ATCC 21834. J Bacteriol 179, 1946-1950.
43. Kai, M., Yano, T., Tamegai, H., Fukumori, Y. & Yamanaka, T. (1992). Thiobacillus ferrooxidans cytochrome c oxidase: purification, and molecular and enzymatic features. J Biochem 112, 816-821.
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 Microbiol 53, 113-119.
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 Microbiol 50, 511-516.
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 Chem 267, 11242-11247.
47. Leduc, L. G. & Ferroni, G. D. (1994). The chemolithotrophic bacterium Thiobacillus ferrooxidans. FEMS Microbiol Lett 14, 103-120.
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 Bacteriol 182, 2269-2276.
49. Lovenberg, W., Buchanan, B. B. & Rabinowitz, J. C. (1963). Studies on the chemical nature of clostridial ferredoxin. J Biol Chem 238, 3899-3913.
50. 8 depending on the ambient redox potential. Biochemistry 36, 12183-12188.
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. Biochemistry 41, 14028-14032.
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 Microbiol 19, 91-95.
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, pp. 219-227. Edited by M. A. Innis, D. H. Gelfand, J. J. Sninsky & T. J. White. San Diego: Academic Press.
54. Palmer, T. & Berks, B. C. (2003). Moving folded proteins across the bacterial cell membrane. Microbiology 149, 547-556.
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. Biochemistry 38, 1276-1283.
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 of Rubrivivax gelatinosus. Biochemistry 34, 11736-11742.
57. Selenska-Pobell, S., Otto, A. & Kutschke, S. (1998). Identification and discrimination of thiobacilli using ARDREA, RAPD and repAPD. J Appl Microbiol 84, 1085-1091.
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 in Escherichia coli. J Biochem 126, 917-926.
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 Chem 277, 28380-28383.
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 Chem 254, 1495-1500.
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 Biophys 239, 94-101.
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 Genomics 4, 51. doi:10.1186/1471-2164-4-51
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 Evol 57, 181-199.
64. 8 as alternative electron donors to the reaction center of Chromatium vinosum. Biochemistry 41, 8868-8875.
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 Biotechnol 2, 179-189.
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 Lett 17, 401-413.
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 Bacteriol 184, 313-317.
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. Microbiology 150, 2113-2123.