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. 1994 Mar;58(1):39–55. doi: 10.1128/mr.58.1.39-55.1994

Molecular genetics of Thiobacillus ferrooxidans.

D E Rawlings 1, T Kusano 1
PMCID: PMC372952  PMID: 8177170

Abstract

Thiobacillus ferrooxidans is a gram-negative, highly acidophilic (pH 1.5 to 2.0), autotrophic bacterium that obtains its energy through the oxidation of ferrous iron or reduced inorganic sulfur compounds. It is usually dominant in the mixed bacterial populations that are used industrially for the extraction of metals such as copper and uranium from their ores. More recently, these bacterial consortia have been used for the biooxidation of refractory gold-bearing arsenopyrite ores prior to the recovery of gold by cyanidation. The commercial use of T. ferrooxidans has led to an increasing interest in the genetics and molecular biology of the bacterium. Initial investigations were aimed at determining whether the unique physiology and specialized habitat of T. ferrooxidans had been accompanied by a high degree of genetic drift from other gram-negative bacteria. Early genetic studies were comparative in nature and concerned the isolation of genes such as nifHDK, glnA, and recA, which are widespread among bacteria. From a molecular biology viewpoint, T. ferrooxidans appears to be a typical member of the proteobacteria. In most instances, cloned gene promoters and protein products have been functional in Escherichia coli. Although T. ferrooxidans has proved difficult to transform with DNA, research on indigenous plasmids and the isolation of the T. ferrooxidans merA gene have resulted in the development of a low-efficiency electroporation system for one strain of T. ferrooxidans. The most recent studies have focused on the molecular genetics of the pathways associated with nitrogen metabolism, carbon dioxide fixation, and components of the energy-producing mechanisms.

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Selected References

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  1. Albright L. M., Ronson C. W., Nixon B. T., Ausubel F. M. Identification of a gene linked to Rhizobium meliloti ntrA whose product is homologous to a family to ATP-binding proteins. J Bacteriol. 1989 Apr;171(4):1932–1941. doi: 10.1128/jb.171.4.1932-1941.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Apel W. A., Dugan P. R., Tuttle J. H. Adenosine 5'-triphosphate formation in Thiobacillus ferrooxidans vesicles by H+ ion gradients comparable to those of environmental conditions. J Bacteriol. 1980 Apr;142(1):295–301. doi: 10.1128/jb.142.1.295-301.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baldi F., Olson G. J. Effects of Cinnabar on Pyrite Oxidation by Thiobacillus ferrooxidans and Cinnabar Mobilization by a Mercury-Resistant Strain. Appl Environ Microbiol. 1987 Apr;53(4):772–776. doi: 10.1128/aem.53.4.772-776.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barros M. E., Rawlings D. E., Woods D. R. Cloning and expression of the Thiobacillus ferrooxidans glutamine synthetase gene in Escherichia coli. J Bacteriol. 1985 Dec;164(3):1386–1389. doi: 10.1128/jb.164.3.1386-1389.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barros M. E., Rawlings D. E., Woods D. R. Mixotrophic Growth of a Thiobacillus ferrooxidans Strain. Appl Environ Microbiol. 1984 Mar;47(3):593–595. doi: 10.1128/aem.47.3.593-595.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berger D. K., Woods D. R., Rawlings D. E. Complementation of Escherichia coli sigma 54 (NtrA)-dependent formate hydrogenlyase activity by a cloned Thiobacillus ferrooxidans ntrA gene. J Bacteriol. 1990 Aug;172(8):4399–4406. doi: 10.1128/jb.172.8.4399-4406.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Birkmann A., Sawers R. G., Böck A. Involvement of the ntrA gene product in the anaerobic metabolism of Escherichia coli. Mol Gen Genet. 1987 Dec;210(3):535–542. doi: 10.1007/BF00327209. [DOI] [PubMed] [Google Scholar]
  8. Bissonnette L., Champetier S., Buisson J. P., Roy P. H. Characterization of the nonenzymatic chloramphenicol resistance (cmlA) gene of the In4 integron of Tn1696: similarity of the product to transmembrane transport proteins. J Bacteriol. 1991 Jul;173(14):4493–4502. doi: 10.1128/jb.173.14.4493-4502.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Blake R. C., 2nd, White K. J., Shute E. A. Effect of divers anions on the electron-transfer reaction between iron and rusticyanin from Thiobacillus ferrooxidans. Biochemistry. 1991 Oct 1;30(39):9443–9449. doi: 10.1021/bi00103a008. [DOI] [PubMed] [Google Scholar]
  10. Brierley C. L. Bacterial leaching. CRC Crit Rev Microbiol. 1978;6(3):207–26I. doi: 10.3109/10408417809090623. [DOI] [PubMed] [Google Scholar]
  11. Brown J. W., Haas E. S., James B. D., Hunt D. A., Liu J. S., Pace N. R. Phylogenetic analysis and evolution of RNase P RNA in proteobacteria. J Bacteriol. 1991 Jun;173(12):3855–3863. doi: 10.1128/jb.173.12.3855-3863.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cobley J. G., Cox J. C. Energy conservation in acidophilic bacteria. Microbiol Rev. 1983 Dec;47(4):579–595. doi: 10.1128/mr.47.4.579-595.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cobley J. G., Haddock B. A. The respiratory chain of Thiobacillus ferrooxidans: the reduction of cytochromes by Fe2+ and the preliminary characterization of rusticyanin a novel "blue" copper protein. FEBS Lett. 1975 Dec 1;60(1):29–33. doi: 10.1016/0014-5793(75)80411-x. [DOI] [PubMed] [Google Scholar]
  14. Cox J. C., Boxer D. H. The purification and some properties of rusticyanin, a blue copper protein involved in iron(II) oxidation from Thiobacillus ferro-oxidans. Biochem J. 1978 Aug 15;174(2):497–502. doi: 10.1042/bj1740497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cox J. C., Nicholls D. G., Ingledew W. J. Transmembrane electrical potential and transmembrane pH gradient in the acidophile Thiobacillus ferro-oxidans. Biochem J. 1979 Jan 15;178(1):195–200. doi: 10.1042/bj1780195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Davidson M. S., Summers A. O. Wide-host-range plasmids function in the genus thiobacillus. Appl Environ Microbiol. 1983 Sep;46(3):565–572. doi: 10.1128/aem.46.3.565-572.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dorrington R. A., Bardien S., Rawlings D. E. The broad-host-range plasmid pTF-FC2 requires a primase-like protein for autonomous replication in Escherichia coli. Gene. 1991 Dec 1;108(1):7–14. doi: 10.1016/0378-1119(91)90481-p. [DOI] [PubMed] [Google Scholar]
  18. Dorrington R. A., Rawlings D. E. Characterization of the minimum replicon of the broad-host-range plasmid pTF-FC2 and similarity between pTF-FC2 and the IncQ plasmids. J Bacteriol. 1990 Oct;172(10):5697–5705. doi: 10.1128/jb.172.10.5697-5705.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dorrington R. A., Rawlings D. E. Identification and sequence of the basic replication region of a broad-host-range plasmid isolated from Thiobacillus ferrooxidans. J Bacteriol. 1989 May;171(5):2735–2739. doi: 10.1128/jb.171.5.2735-2739.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Drobner E., Huber H., Stetter K. O. Thiobacillus ferrooxidans, a facultative hydrogen oxidizer. Appl Environ Microbiol. 1990 Sep;56(9):2922–2923. doi: 10.1128/aem.56.9.2922-2923.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Drolet M., Lau P. C. Mobilization protein-DNA binding and divergent transcription at the transfer origin of the Thiobacillus ferrooxidans pTF1 plasmid. Mol Microbiol. 1992 Apr;6(8):1061–1071. doi: 10.1111/j.1365-2958.1992.tb02171.x. [DOI] [PubMed] [Google Scholar]
  22. Drolet M., Zanga P., Lau P. C. The mobilization and origin of transfer regions of a Thiobacillus ferrooxidans plasmid: relatedness to plasmids RSF1010 and pSC101. Mol Microbiol. 1990 Aug;4(8):1381–1391. doi: 10.1111/j.1365-2958.1990.tb00717.x. [DOI] [PubMed] [Google Scholar]
  23. Grinsted J., de la Cruz F., Schmitt R. The Tn21 subgroup of bacterial transposable elements. Plasmid. 1990 Nov;24(3):163–189. doi: 10.1016/0147-619x(90)90001-s. [DOI] [PubMed] [Google Scholar]
  24. Harrison A. P., Jr The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. Annu Rev Microbiol. 1984;38:265–292. doi: 10.1146/annurev.mi.38.100184.001405. [DOI] [PubMed] [Google Scholar]
  25. Henikoff S., Haughn G. W., Calvo J. M., Wallace J. C. A large family of bacterial activator proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6602–6606. doi: 10.1073/pnas.85.18.6602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Holden P. J., Brown R. W. Amplification of ribulose biphosphate carboxylase/oxygenase large subunit (RuBisCO LSU) gene fragments from Thiobacillus ferrooxidans and a moderate thermophile using polymerase chain reaction. FEMS Microbiol Rev. 1993 Jul;11(1-3):19–30. doi: 10.1111/j.1574-6976.1993.tb00262.x. [DOI] [PubMed] [Google Scholar]
  27. Holmes D. S., Lobos J. H., Bopp L. H., Welch G. C. Cloning of a Thiobacillus ferrooxidans plasmid in Escherichia coli. J Bacteriol. 1984 Jan;157(1):324–326. doi: 10.1128/jb.157.1.324-326.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hoover T. R., Santero E., Porter S., Kustu S. The integration host factor stimulates interaction of RNA polymerase with NIFA, the transcriptional activator for nitrogen fixation operons. Cell. 1990 Oct 5;63(1):11–22. doi: 10.1016/0092-8674(90)90284-l. [DOI] [PubMed] [Google Scholar]
  29. Ingledew W. J. Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta. 1982 Nov 30;683(2):89–117. doi: 10.1016/0304-4173(82)90007-6. [DOI] [PubMed] [Google Scholar]
  30. Inoue C., Sugawara K., Kusano T. The merR regulatory gene in Thiobacillus ferrooxidans is spaced apart from the mer structural genes. Mol Microbiol. 1991 Nov;5(11):2707–2718. doi: 10.1111/j.1365-2958.1991.tb01979.x. [DOI] [PubMed] [Google Scholar]
  31. Inoue C., Sugawara K., Kusano T. Thiobacillus ferrooxidans mer operon: sequence analysis of the promoter and adjacent genes. Gene. 1990 Nov 30;96(1):115–120. doi: 10.1016/0378-1119(90)90349-v. [DOI] [PubMed] [Google Scholar]
  32. Inoue C., Sugawara K., Shiratori T., Kusano T., Kitagawa Y. Nucleotide sequence of the Thiobacillus ferrooxidans chromosomal gene encoding mercuric reductase. Gene. 1989 Dec 7;84(1):47–54. doi: 10.1016/0378-1119(89)90138-8. [DOI] [PubMed] [Google Scholar]
  33. Jerez C. A., Seeger M., Amaro A. M. Phosphate starvation affects the synthesis of outer membrane proteins in Thiobacillus ferrooxidans. FEMS Microbiol Lett. 1992 Nov 1;77(1-3):29–33. doi: 10.1016/0378-1097(92)90127-a. [DOI] [PubMed] [Google Scholar]
  34. Jin S. M., Yan W. M., Wang Z. N. Transfer of IncP Plasmids to Extremely Acidophilic Thiobacillus thiooxidans. Appl Environ Microbiol. 1992 Jan;58(1):429–430. doi: 10.1128/aem.58.1.429-430.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kai M., Yano T., Fukumori Y., Yamanaka T. Cytochrome oxidase of an acidophilic iron-oxidizing bacterium, Thiobacillus ferrooxidans, functions at pH 3.5. Biochem Biophys Res Commun. 1989 Apr 28;160(2):839–843. doi: 10.1016/0006-291x(89)92510-2. [DOI] [PubMed] [Google Scholar]
  36. Kawaguchi H., Inagaki K., Kuwata Y., Tanaka H., Tano T. 3-Isopropylmalate dehydrogenase from chemolithoautotroph Thiobacillus ferrooxidans: DNA sequence, enzyme purification, and characterization. J Biochem. 1993 Sep;114(3):370–377. doi: 10.1093/oxfordjournals.jbchem.a124183. [DOI] [PubMed] [Google Scholar]
  37. Keener J., Kustu S. Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC. Proc Natl Acad Sci U S A. 1988 Jul;85(14):4976–4980. doi: 10.1073/pnas.85.14.4976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kelly D. P. Physiology of the thiobacilli: elucidating the sulphur oxidation pathway. Microbiol Sci. 1985;2(4):105–109. [PubMed] [Google Scholar]
  39. Kim Y. J., Lin L. S., Meyer R. J. Two domains at the origin are required for replication and maintenance of broad-host-range plasmid R1162. J Bacteriol. 1987 Dec;169(12):5870–5872. doi: 10.1128/jb.169.12.5870-5872.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kulpa C. F., Roskey M. T., Travis M. T. Transfer of plasmid RP1 into chemolithotrophic Thiobacillus neapolitanus. J Bacteriol. 1983 Oct;156(1):434–436. doi: 10.1128/jb.156.1.434-436.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kusano T., Ji G. Y., Inoue C., Silver S. Constitutive synthesis of a transport function encoded by the Thiobacillus ferrooxidans merC gene cloned in Escherichia coli. J Bacteriol. 1990 May;172(5):2688–2692. doi: 10.1128/jb.172.5.2688-2692.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kusano T., Sugawara K., Inoue C., Takeshima T., Numata M., Shiratori T. Electrotransformation of Thiobacillus ferrooxidans with plasmids containing a mer determinant. J Bacteriol. 1992 Oct;174(20):6617–6623. doi: 10.1128/jb.174.20.6617-6623.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kusano T., Sugawara K. Specific binding of Thiobacillus ferrooxidans RbcR to the intergenic sequence between the rbc operon and the rbcR gene. J Bacteriol. 1993 Feb;175(4):1019–1025. doi: 10.1128/jb.175.4.1019-1025.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kusano T., Takeshima T., Inoue C., Sugawara K. Evidence for two sets of structural genes coding for ribulose bisphosphate carboxylase in Thiobacillus ferrooxidans. J Bacteriol. 1991 Nov;173(22):7313–7323. doi: 10.1128/jb.173.22.7313-7323.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kusano T., Takeshima T., Inoue C., Sugawara K. Identification of the purA gene encoding adenylosuccinate synthetase in Thiobacillus ferrooxidans. Curr Microbiol. 1993 Apr;26(4):197–204. doi: 10.1007/BF01577377. [DOI] [PubMed] [Google Scholar]
  46. Kusano T., Takeshima T., Sugawara K., Inoue C., Shiratori T., Yano T., Fukumori Y., Yamanaka T. Molecular cloning of the gene encoding Thiobacillus ferrooxidans Fe(II) oxidase. High homology of the gene product with HiPIP. J Biol Chem. 1992 Jun 5;267(16):11242–11247. [PubMed] [Google Scholar]
  47. Lane D. J., Harrison A. P., Jr, Stahl D., Pace B., Giovannoni S. J., Olsen G. J., Pace N. R. Evolutionary relationships among sulfur- and iron-oxidizing eubacteria. J Bacteriol. 1992 Jan;174(1):269–278. doi: 10.1128/jb.174.1.269-278.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Lane D. J., Stahl D. A., Olsen G. J., Heller D. J., Pace N. R. Phylogenetic analysis of the genera Thiobacillus and Thiomicrospira by 5S rRNA sequences. J Bacteriol. 1985 Jul;163(1):75–81. doi: 10.1128/jb.163.1.75-81.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Leyh T. S., Taylor J. C., Markham G. D. The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J Biol Chem. 1988 Feb 15;263(5):2409–2416. [PubMed] [Google Scholar]
  50. Lin L. S., Kim Y. J., Meyer R. J. The 20 bp, directly repeated DNA sequence of broad host range plasmid R1162 exerts incompatibility in vivo and inhibits R1162 DNA replication in vitro. Mol Gen Genet. 1987 Jul;208(3):390–397. doi: 10.1007/BF00328129. [DOI] [PubMed] [Google Scholar]
  51. Lundgren D. G., Silver M. Ore leaching by bacteria. Annu Rev Microbiol. 1980;34:263–283. doi: 10.1146/annurev.mi.34.100180.001403. [DOI] [PubMed] [Google Scholar]
  52. Martin P. A., Dugan P. R., Tuovinen O. H. Plasmid DNA in acidophilic, chemolithotrophic thiobacilli. Can J Microbiol. 1981 Aug;27(8):850–853. doi: 10.1139/m81-133. [DOI] [PubMed] [Google Scholar]
  53. Ninfa A. J., Magasanik B. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5909–5913. doi: 10.1073/pnas.83.16.5909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Nunzi F., Woudstra M., Campèse D., Bonicel J., Morin D., Bruschi M. Amino-acid sequence of rusticyanin from Thiobacillus ferrooxidans and its comparison with other blue copper proteins. Biochim Biophys Acta. 1993 Mar 5;1162(1-2):28–34. doi: 10.1016/0167-4838(93)90123-9. [DOI] [PubMed] [Google Scholar]
  55. Olson G. J., Porter F. D., Rubinstein J., Silver S. Mercuric reductase enzyme from a mercury-volatilizing strain of Thiobacillus ferrooxidans. J Bacteriol. 1982 Sep;151(3):1230–1236. doi: 10.1128/jb.151.3.1230-1236.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Pretorius I. M., Rawlings D. E., O'Neill E. G., Jones W. A., Kirby R., Woods D. R. Nucleotide sequence of the gene encoding the nitrogenase iron protein of Thiobacillus ferrooxidans. J Bacteriol. 1987 Jan;169(1):367–370. doi: 10.1128/jb.169.1.367-370.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pretorius I. M., Rawlings D. E., Woods D. R. Identification and cloning of Thiobacillus ferrooxidans structural nif genes in Escherichia coli. Gene. 1986;45(1):59–65. doi: 10.1016/0378-1119(86)90132-0. [DOI] [PubMed] [Google Scholar]
  58. Pronk J. T., Liem K., Bos P., Kuenen J. G. Energy Transduction by Anaerobic Ferric Iron Respiration in Thiobacillus ferrooxidans. Appl Environ Microbiol. 1991 Jul;57(7):2063–2068. doi: 10.1128/aem.57.7.2063-2068.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Pronk J. T., Meijer W. M., Hazeu W., van Dijken J. P., Bos P., Kuenen J. G. Growth of Thiobacillus ferrooxidans on Formic Acid. Appl Environ Microbiol. 1991 Jul;57(7):2057–2062. doi: 10.1128/aem.57.7.2057-2062.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Pulgar V., Gaete L., Allende J., Orellana O., Jordana X., Jedlicki E. Isolation and nucleotide sequence of the Thiobacillus ferrooxidans genes for the small and large subunits of ribulose 1,5-bisphosphate carboxylase/oxygenase. FEBS Lett. 1991 Nov 4;292(1-2):85–89. doi: 10.1016/0014-5793(91)80840-y. [DOI] [PubMed] [Google Scholar]
  61. Ramesar R. S., Abratt V., Woods D. R., Rawlings D. E. Nucleotide sequence and expression of a cloned Thiobacillus ferrooxidans recA gene in Escherichia coli. Gene. 1989 May 15;78(1):1–8. doi: 10.1016/0378-1119(89)90308-9. [DOI] [PubMed] [Google Scholar]
  62. Ramesar R. S., Woods D. R., Rawlings D. E. Cloning and expression in Escherichia coli of a recA-like gene from the acidophilic autotroph Thiobacillus ferrooxidans. J Gen Microbiol. 1988 May;134(5):1141–1146. doi: 10.1099/00221287-134-5-1141. [DOI] [PubMed] [Google Scholar]
  63. Rawlings D. E., Jones W. A., O'Neill E. G., Woods D. R. Nucleotide sequence of the glutamine synthetase gene and its controlling region from the acidophilic autotroph Thiobacillus ferrooxidans. Gene. 1987;53(2-3):211–217. doi: 10.1016/0378-1119(87)90009-6. [DOI] [PubMed] [Google Scholar]
  64. Rawlings D. E., Pretorius I., Woods D. R. Expression of a Thiobacillus ferrooxidans origin of replication in Escherichia coli. J Bacteriol. 1984 May;158(2):737–738. doi: 10.1128/jb.158.2.737-738.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Rawlings D. E. Sequence and structural analysis of the alpha- and beta-dinitrogenase subunits of Thiobacillus ferrooxidans. Gene. 1988 Sep 30;69(2):337–343. doi: 10.1016/0378-1119(88)90444-1. [DOI] [PubMed] [Google Scholar]
  66. Rawlings D. E., Woods D. R. Mobilization of Thiobacillus ferrooxidans plasmids among Escherichia coli strains. Appl Environ Microbiol. 1985 May;49(5):1323–1325. doi: 10.1128/aem.49.5.1323-1325.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Reitzer L. J., Magasanik B. Expression of glnA in Escherichia coli is regulated at tandem promoters. Proc Natl Acad Sci U S A. 1985 Apr;82(7):1979–1983. doi: 10.1073/pnas.82.7.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Rohrer J., Rawlings D. E. Sequence analysis and characterization of the mobilization region of a broad-host-range plasmid, pTF-FC2, isolated from Thiobacillus ferrooxidans. J Bacteriol. 1992 Oct;174(19):6230–6237. doi: 10.1128/jb.174.19.6230-6237.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Ronk M., Shively J. E., Shute E. A., Blake R. C., 2nd Amino acid sequence of the blue copper protein rusticyanin from Thiobacillus ferrooxidans. Biochemistry. 1991 Oct 1;30(39):9435–9442. doi: 10.1021/bi00103a007. [DOI] [PubMed] [Google Scholar]
  70. Salazar O., Takamiya M., Orellana O. Characterization of the two rRNA gene operons present in Thiobacillus ferrooxidans. FEBS Lett. 1989 Jan 2;242(2):439–443. doi: 10.1016/0014-5793(89)80518-6. [DOI] [PubMed] [Google Scholar]
  71. Sato A., Fukumori Y., Yano T., Kai M., Yamanaka T. Thiobacillus ferrooxidans cytochrome c-552: purification and some of its molecular features. Biochim Biophys Acta. 1989 Sep 28;976(2-3):129–134. doi: 10.1016/s0005-2728(89)80221-x. [DOI] [PubMed] [Google Scholar]
  72. Scholz P., Haring V., Wittmann-Liebold B., Ashman K., Bagdasarian M., Scherzinger E. Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene. 1989 Feb 20;75(2):271–288. doi: 10.1016/0378-1119(89)90273-4. [DOI] [PubMed] [Google Scholar]
  73. Schrader J. A., Holmes D. S. Phenotypic switching of Thiobacillus ferrooxidans. J Bacteriol. 1988 Sep;170(9):3915–3923. doi: 10.1128/jb.170.9.3915-3923.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Senior A. E. The proton-translocating ATPase of Escherichia coli. Annu Rev Biophys Biophys Chem. 1990;19:7–41. doi: 10.1146/annurev.bb.19.060190.000255. [DOI] [PubMed] [Google Scholar]
  75. Shiratori T., Inoue C., Sugawara K., Kusano T., Kitagawa Y. Cloning and expression of Thiobacillus ferrooxidans mercury ion resistance genes in Escherichia coli. J Bacteriol. 1989 Jun;171(6):3458–3464. doi: 10.1128/jb.171.6.3458-3464.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Silver S., Walderhaug M. Gene regulation of plasmid- and chromosome-determined inorganic ion transport in bacteria. Microbiol Rev. 1992 Mar;56(1):195–228. doi: 10.1128/mr.56.1.195-228.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Sugio T., Domatsu C., Munakata O., Tano T., Imai K. Role of a Ferric Ion-Reducing System in Sulfur Oxidation of Thiobacillus ferrooxidans. Appl Environ Microbiol. 1985 Jun;49(6):1401–1406. doi: 10.1128/aem.49.6.1401-1406.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Sugio T., Hirayama K., Inagaki K., Tanaka H., Tano T. Molybdenum oxidation by Thiobacillus ferrooxidans. Appl Environ Microbiol. 1992 May;58(5):1768–1771. doi: 10.1128/aem.58.5.1768-1771.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Sugio T., White K. J., Shute E., Choate D., Blake R. C. Existence of a hydrogen sulfide:ferric ion oxidoreductase in iron-oxidizing bacteria. Appl Environ Microbiol. 1992 Jan;58(1):431–433. doi: 10.1128/aem.58.1.431-433.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Takamiya M., Salazar O., Vargas D., Jedlicki E., Orellana O. Identification and structural analysis of a ribosomal RNA gene promoter from Thiobacillus ferrooxidans. FEBS Lett. 1990 Oct 15;272(1-2):50–54. doi: 10.1016/0014-5793(90)80446-p. [DOI] [PubMed] [Google Scholar]
  81. Takeshima T., Inoue C., Kitagawa Y., Kusano T. Nucleotide sequence of a Thiobacillus ferrooxidans chromosomal gene, which encodes putative RNA component of RNase P. Nucleic Acids Res. 1989 Nov 25;17(22):9482–9482. doi: 10.1093/nar/17.22.9482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Toukdarian A., Kennedy C. Regulation of nitrogen metabolism in Azotobacter vinelandii: isolation of ntr and glnA genes and construction of ntr mutants. EMBO J. 1986 Feb;5(2):399–407. doi: 10.1002/j.1460-2075.1986.tb04225.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Tuovinen O. H., Niemelä S. I., Gyllenberg H. G. Tolerance of Thiobacillus ferrooxidans to some metals. Antonie Van Leeuwenhoek. 1971;37(4):489–496. doi: 10.1007/BF02218519. [DOI] [PubMed] [Google Scholar]
  84. Tyler B. Regulation of the assimilation of nitrogen compounds. Annu Rev Biochem. 1978;47:1127–1162. doi: 10.1146/annurev.bi.47.070178.005403. [DOI] [PubMed] [Google Scholar]
  85. Venegas A., Hevia E., Sánchez H. Sequence of two tRNA genes from a Thiobacillus ferrooxidans ribosomal operon. Nucleic Acids Res. 1988 Aug 25;16(16):8179–8179. doi: 10.1093/nar/16.16.8179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Walker G. C. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev. 1984 Mar;48(1):60–93. doi: 10.1128/mr.48.1.60-93.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Walker J. E., Fearnley I. M., Lutter R., Todd R. J., Runswick M. J. Structural aspects of proton-pumping ATPases. Philos Trans R Soc Lond B Biol Sci. 1990 Jan 30;326(1236):367–378. doi: 10.1098/rstb.1990.0018. [DOI] [PubMed] [Google Scholar]
  88. Wheatcroft R., Laberge S. Identification and nucleotide sequence of Rhizobium meliloti insertion sequence ISRm3: similarity between the putative transposase encoded by ISRm3 and those encoded by Staphylococcus aureus IS256 and Thiobacillus ferrooxidans IST2. J Bacteriol. 1991 Apr;173(8):2530–2538. doi: 10.1128/jb.173.8.2530-2538.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Yakobson E., Deiss C., Hirata K., Guiney D. G. Initiation of DNA synthesis in the transfer origin region of RK2 by the plasmid-encoded primase: detection using defective M13 phage. Plasmid. 1990 Jan;23(1):80–84. doi: 10.1016/0147-619x(90)90048-h. [DOI] [PubMed] [Google Scholar]
  91. Yates J. R., Cunningham R. P., Holmes D. S. IST2: an insertion sequence from Thiobacillus ferrooxidans. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7284–7287. doi: 10.1073/pnas.85.19.7284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Yates J. R., Holmes D. S. Two families of repeated DNA sequences in Thiobacillus ferrooxidans. J Bacteriol. 1987 May;169(5):1861–1870. doi: 10.1128/jb.169.5.1861-1870.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Young S., Bolton P., Dyson M., Harvey W., Diamantopoulos C. Macrophage responsiveness to light therapy. Lasers Surg Med. 1989;9(5):497–505. doi: 10.1002/lsm.1900090513. [DOI] [PubMed] [Google Scholar]
  94. Ziegelin G., Pansegrau W., Strack B., Balzer D., Kröger M., Kruft V., Lanka E. Nucleotide sequence and organization of genes flanking the transfer origin of promiscuous plasmid RP4. DNA Seq. 1991;1(5):303–327. doi: 10.3109/10425179109020786. [DOI] [PubMed] [Google Scholar]

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