1887

Abstract

Autotrophic acidophilic iron- and sulfur-oxidizing bacteria of the genus constitute a heterogeneous taxon encompassing a high degree of diversity at the phylogenetic and genetic levels, though currently only two species are recognized ( and ). One of the major functional disparities concerns the biochemical mechanisms of iron and sulfur oxidation, with discrepancies reported in the literature concerning the genes and proteins involved in these processes. These include two types of high-potential iron–sulfur proteins (HiPIPs): (i) Iro, which has been described as the iron oxidase; and (ii) Hip, which has been proposed to be involved in the electron transfer between sulfur compounds and oxygen. In addition, two rusticyanins have been described: (i) rusticyanin A, encoded by the gene and belonging to the well-characterized operon, which plays a central role in the iron respiratory chain; and (ii) rusticyanin B, a protein to which no function has yet been ascribed. Data from a multilocus sequence analysis of 21 strains of Fe(II)-oxidizing acidithiobacilli obtained from public and private collections using five phylogenetic markers showed that these strains could be divided into four monophyletic groups. These divisions correlated not only with levels of genomic DNA hybridization and phenotypic differences among the strains, but also with the types of rusticyanin and HiPIPs that they harbour. Taken together, the data indicate that Fe(II)-oxidizing acidithiobacilli comprise at least four distinct taxa, all of which are able to oxidize both ferrous iron and sulfur, and suggest that different iron oxidation pathways have evolved in these closely related bacteria.

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2011-01-01
2024-03-29
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References

  1. Akbar T., Akhtar K., Ghauri M. A., Anwar M. A., Rehman M., Rehman M., Zafar Y., Khalib A. M. 2005; Relationship among acidophilic bacteria from diverse environments as determined by randomly amplified polymorphic DNA analysis (RAPD. World J Microbiol Biotechnol 21:645–648
    [Google Scholar]
  2. Amils R., Irazabal N., Moreira D., Abad J. P., Marin I. 1998; Genomic organization analysis of acidophilic chemolithotrophic bacteria using pulsed field gel electrophoretic techniques. Biochimie 80:911–921
    [Google Scholar]
  3. Appia-Ayme C., Guiliani N., Ratouchniak J., Bonnefoy V. 1999; Characterization of an operon encoding two c -type cytochromes, an aa 3-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65:4781–4787
    [Google Scholar]
  4. 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 ATCC33020 strain. Biochim Biophys Acta 144399–112
    [Google Scholar]
  5. Bergamo R. F., Novo M. T., Verissimo R. V., Paulino L. C., Stoppe N. C., Sato M. I., Manfio G. P., Prado P. I., Garcia O. Jr, Ottoboni L. M. 2004; Differentiation of Acidithiobacillus ferrooxidans and A. thiooxidans strains based on 16S–23S rDNA spacer polymorphism analysis. Res Microbiol 155:559–567
    [Google Scholar]
  6. Blake R. C., Johnson D. B. 2000; Phylogenetic and biochemical diversity among acidophilic bacteria that respire on iron. In Environmental Microbe–Metal Interactions pp 53–78 Edited by Lovley D. R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  7. Brauckmann B. 1985; Autotrophe und heterotrophe Bakterien im Biotop “Altes Lager Erzbergwerk Rammelsberg” und ihr Einfluss auf die Laugung sulfidischer Mischerze . PhD thesis Universität Braunschweig; Braunschweig, Germany:
    [Google Scholar]
  8. Bruscella P., Cassagnaud L., Ratouchniak J., Brasseur G., Lojou E., Amils R., Bonnefoy V. 2005; 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 151:1421–1431
    [Google Scholar]
  9. Bruscella P., Appia-Ayme C., Levican G., Ratouchniak J., Jedlicki E., Holmes D. S., Bonnefoy V. 2007; Differential expression of two bc 1 complexes in the strict acidophilic chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans suggests a model for their respective roles in iron or sulfur oxidation. Microbiology 153:102–110
    [Google Scholar]
  10. Cashion P., Holder-Franklin M. A., McCully J., Franklin M. 1977; A rapid method for the base ratio determination of bacterial DNA. Anal Biochem 81:461–466
    [Google Scholar]
  11. 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
    [Google Scholar]
  12. Chen H., Yang B., Chen X. 2009; Identification and characterization of four strains of Acidithiobacillus ferrooxidans isolated from different sites in China. Microbiol Res 164:613–623
    [Google Scholar]
  13. Dave S. R., Gupta K. H., Tipre D. R. 2008; Characterization of arsenic resistant and arsenopyrite oxidizing Acidithiobacillus ferrooxidans from Hutti gold leachate and effluents. Bioresour Technol 99:7514–7520
    [Google Scholar]
  14. De Ley J., Cattoir H., Reynaerts A. 1970; The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142
    [Google Scholar]
  15. Dispirito A. A., Silver M., Voss L., Tuovinen O. H. 1982; Flagella and pili of iron-oxidizing Thiobacilli isolated from a uranium mine in Northern Ontario, Canada. Appl Environ Microbiol 43:1196–1200
    [Google Scholar]
  16. Duquesne K., Lebrun S., Casiot C., Bruneel O., Personne 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
    [Google Scholar]
  17. Egal M., Casiot C., Morin G., Parmentier M., Bruneel O., Lebrun S., Elbaz-Poulichet F. 2009; Kinetic control on the formation of tooeleite, schwertmannite and jarosite by Acidithiobacillus ferrooxidans strains in an As(III)-rich acid mine water. Chem Geol 265:432–441
    [Google Scholar]
  18. Fukumori Y., Yano T., Sato A., Yamanaka T. 1988; Fe(II) oxidizing enzyme purified from Thiobacillus ferrooxidans . FEMS Microbiol Lett 50:169–172
    [Google Scholar]
  19. Guo Y., Zheng W., Rong X., Huang Y. 2008; A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 58:149–159
    [Google Scholar]
  20. Hallberg K. B., Coupland K., Kimura S., Johnson D. B. 2006; Macroscopic streamer growths in acidic, metal-rich mine waters in north Wales consist of novel and remarkably simple bacterial communities. Appl Environ Microbiol 72:2022–2030
    [Google Scholar]
  21. Hallberg K. B., Amouric A., Brochier-Armanet C., Bonnefoy V., Johnson D. B. 2009; Physiological and phylogenetic heterogeneity among iron-oxidizing Acidithiobacillus spp., and characteristics of the novel species Acidithiobacillus ferrivorans . Adv Mat Res 71:73167–170
    [Google Scholar]
  22. Hallberg K. B., Gonzalez-Toril E., Johnson D. B. 2010; Acidithiobacillus ferrivorans , sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 14:9–19
    [Google Scholar]
  23. Harneit K., Göksel A., Kock D., Klock J.-H., Gehrke T., Sand W. 2006; Adhesion to metal sulfide surfaces by cells of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans and Leptospirillum ferrooxidans . Hydrometallurgy 83:245–254
    [Google Scholar]
  24. 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
    [Google Scholar]
  25. Harrison A. P. Jr 1984; The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. Annu Rev Microbiol 38:265–292
    [Google Scholar]
  26. Hippe H. 2000; Leptospirillum gen. nov. (ex Markosyan 1972), nom. rev., including Leptospirillum ferrooxidans sp. nov. (ex Markosyan 1972), nom. rev. and Leptospirillum thermoferrooxidans sp. nov. (Golovacheva et al. 1992. Int J Syst Evol Microbiol 50:501–503
    [Google Scholar]
  27. Holmes D., Bonnefoy V. 2007; Genetic and bioinformatic insights into iron and sulfur oxidation mechanisms of bioleaching organisms. In Biomining pp 281–307 Edited by Rawlings D. E., Johnson D. B. Berlin, Heidelberg: Springer-Verlag;
    [Google Scholar]
  28. Holmes D. E., Nevin K. P., Lovley D. R. 2004; Comparison of 16S rRNA, nifD , recA , gyrB , rpoB and fusA genes within the family Geobacteraceae fam. nov. Int J Syst Evol Microbiol 54:1591–1599
    [Google Scholar]
  29. Huß V. A. R., Festl H., Schleifer K. H. 1983; Studies on the spectrophotometric determination of DNA hybridization from renaturation rates. Syst Appl Microbiol 4:184–192
    [Google Scholar]
  30. Ida C., Sasaki K., Ando K., Blake R. C. II, Saiki H., Ohmura N. 2003; Kinetic rate constant for electron transfer between ferrous ions and novel rusticyanin isoform in Acidithiobacillus ferrooxidans . J Biosci Bioeng 95:534–537
    [Google Scholar]
  31. Jobb G., von Haeseler A., Strimmer K. 2004; treefinder: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18
    [Google Scholar]
  32. Johnson D. B., Hallberg K. B. 2007; Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. In Biomining pp 237–261 Edited by Rawlings D. E., Johnson D. B. Berlin: Springer-Verlag;
    [Google Scholar]
  33. 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
    [Google Scholar]
  34. Kelly D. P., Wood A. P. 2005; Genus Acidithiobacillus . In Bergey's Manual of Systematic Bacteriology pp 60–62 Edited by Brenner D. J., Krieg N. R., Staley J. T. Michigan: Bergey's Manual Trust;
    [Google Scholar]
  35. Kupka D., Rzhepishevska O. I., Dopson M., Lindstrom E. B., Karnachuk O. V., Tuovinen O. H. 2007; Bacterial oxidation of ferrous iron at low temperatures. Biotechnol Bioeng 97:1470–1478
    [Google Scholar]
  36. Kusano T., Takeshima T., Sugawara 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
    [Google Scholar]
  37. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. other authors 2007; clustal w and clustal_x version 2.0. Bioinformatics 23:2947–2948
    [Google Scholar]
  38. Leathen W. W., Braley S. A. 1954; A new iron-oxidizing bacterium: Ferrobacillus ferrooxidans . Bacteriol Proc 195444
    [Google Scholar]
  39. Li Y. Q., Wan D. S., Huang S. S., Leng F. F., Yan L., Ni Y. Q., Li H. Y. 2010; Type IV pili of Acidithiobacillus ferrooxidans are necessary for sliding, twitching motility, and adherence. Curr Microbiol 60:17–24
    [Google Scholar]
  40. 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
    [Google Scholar]
  41. Luo H., Shen L., Yin H., Li Q., Chen Q., Luo Y., Liao L., Qiu G., Liu X. 2009; Comparative genomic analysis of Acidithiobacillus ferrooxidans strains using the A. ferrooxidans ATCC 23270 whole-genome oligonucleotide microarray. Can J Microbiol 55:587–598
    [Google Scholar]
  42. Maiden M. C. 2006; Multilocus sequence typing of bacteria. Annu Rev Microbiol 60:561–588
    [Google Scholar]
  43. Mitchell D., Harneit K., Meyer G., Sand W., Stackebrandt E. 2003; Systematic analysis of our culture collection for “genospecies” of Acidithiobacillus ferrooxidans , Acidithiobacillus thiooxidans and Leptospirillum ferrooxidans . In International Biohydrometallurgy Symposium Athens, Greece:
    [Google Scholar]
  44. Ni Y. Q., Yang Y., Bao J. T., He K. Y., Li H. Y. 2007; Inter- and intraspecific genomic variability of the 16S–23S intergenic spacer regions (ISR) in representatives of Acidithiobacillus thiooxidans and Acidithiobacillus ferrooxidans . FEMS Microbiol Lett 270:58–66
    [Google Scholar]
  45. Ni Y., Wan D., He K. 2008a; 16S rDNA and 16S–23S internal transcribed spacer sequence analyses reveal inter- and intraspecific Acidithiobacillus phylogeny. Microbiology 154:2397–2407
    [Google Scholar]
  46. Ni Y. Q., He K. Y., Bao J. T., Yang Y., Wan D. S., Li H. Y. 2008b; Genomic and phenotypic heterogeneity of Acidithiobacillus spp. strains isolated from diverse habitats in China. FEMS Microbiol Ecol 64:248–259
    [Google Scholar]
  47. Novo M. T. M., De Souza A. P., Garcia Junior O., Ottoboni L. M. 1996; RAPD genomic fingerprinting differentiates Thiobacillus ferrooxidans strains. Syst Appl Microbiol 19:91–95
    [Google Scholar]
  48. Okibe N., Gericke M., Hallberg K. B., Johnson D. B. 2003; Enumeration and characterization of acidophilic microorganisms isolated from a pilot plant stirred-tank bioleaching operation. Appl Environ Microbiol 69:1936–1943
    [Google Scholar]
  49. Paulino L. C., Bergamo R. F., Garcia O. Jr, de Mello M. P., Manfio G. P., Ottoboni L. M. 2001; Molecular characterization of Acidithiobacillus ferrooxidans and A. thiooxidans strains isolated from mine wastes in Brazil. Antonie van Leeuwenhoek 80:65–75
    [Google Scholar]
  50. Peng H., Yang Y., Li X., Qiu G., Liu X., Huang J., Hu Y. 2006; Structure analysis of 16S rDNA sequences from strains of Acidithiobacillus ferrooxidans . J Biochem Mol Biol 39:178–182
    [Google Scholar]
  51. Philippe H. 1993; must, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res 21:5264–5272
    [Google Scholar]
  52. Quatrini R., Appia-Ayme C., Denis Y., Ratouchniak J., Veloso F., Valdes J., Lefimil C., Silver S., Roberto F. other authors 2006; Insights into the iron and sulfur energetic metabolism of Acidithiobacillus ferrooxidans by microarray transcriptome profiling. Hydrometallurgy 83:263–272
    [Google Scholar]
  53. Quatrini R., Appia-Ayme C., Denis Y., Jedlicki E., Holmes D. S., Bonnefoy V. 2009; Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans . BMC Genomics 10:394
    [Google Scholar]
  54. Razzell W. E., Trusell P. C. 1963; Isolation and properties of an iron-oxidizing Thiobacillus . J Bacteriol 85:595–603
    [Google Scholar]
  55. Rivas R., Martens M., de Lajudie P., Willems A. 2009; Multilocus sequence analysis of the genus Bradyrhizobium . Syst Appl Microbiol 32:101–110
    [Google Scholar]
  56. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
    [Google Scholar]
  57. Sand W., Rohde K., Sobotke B., Zenneck C. 1992; Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58:85–92
    [Google Scholar]
  58. Sasaki K., Ida C., Ando A., Matsumoto N., Saiki H., Ohmura N. 2003; Respiratory isozyme, two types of rusticyanin of Acidithiobacillus ferrooxidans . Biosci Biotechnol Biochem 67:1039–1047
    [Google Scholar]
  59. Selenska-Pobell S., Otto A., Kutschke S. 1998; Identification and discrimination of thiobacilli using ARDREA, RAPD and rep-APD. J Appl Microbiol 84:1085–1091
    [Google Scholar]
  60. Stackebrandt E., Goebel B. M. 1994; Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849
    [Google Scholar]
  61. Suzuki I., Takeuchi T. L., Yuthasastrakosol T. D., Oh J. K. 1990; Ferrous iron and sulfur oxidation and ferric iron reduction activities of Thiobacillus ferrooxidans are affected by growth on ferrous iron, sulfur, or a sulfide ore. Appl Environ Microbiol 56:1620–1626
    [Google Scholar]
  62. Takamori T., Kakuta H., Sumiya M. 1983; Some properties of Thiobacillus ferrooxidans and applications of the properties to improvement of the rate of sulfide mineral leaching. In International Symposium on Biohydrometallurgy pp 679–691 Edited by Rossi G, Torma. Calgari, Sardinia, Italy: Associazione Mineraria Sarda; Iglesias, Italy:
    [Google Scholar]
  63. Tomizuka N., Yagisawa M., Someya J., Takahara Y. 1976; Continuous leaching of uranium by Thiobacillus ferrooxidans . Agric Biol Chem 40:1019–1025
    [Google Scholar]
  64. Valdés J., Pedroso I., Quatrini R., Dodson R. J., Tettelin H., Blake R. II, Eisen J. A., Holmes D. S. 2008; Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genomics 9:597
    [Google Scholar]
  65. Wakai S., Kikumoto M., Kanao T., Kamimura K. 2004; Involvement of sulfide : quinone oxidoreductase in sulfur oxidation of an acidophilic iron-oxidizing bacterium, Acidithiobacillus ferrooxidans NASF-1. Biosci Biotechnol Biochem 68:2519–2528
    [Google Scholar]
  66. Wakao N., Hanada K., Takahashi A., Sakurai Y., Shiota H. 1991; Morphological, physiological, and chemotaxonomical characteristics of iron- and sulfur-oxidizing bacteria isolated from acid mine drainage waters. J Gen Appl Microbiol 37:35–48
    [Google Scholar]
  67. Wakeman K., Auvinen H., Johnson D. B. 2008; Microbiological and geochemical dynamics in simulated-heap leaching of a polymetallic sulfide ore. Biotechnol Bioeng 101:739–750
    [Google Scholar]
  68. Waltenbury D. R., Leduc L. G., Ferroni G. D. 2005; The use of RAPD genomic fingerprinting to study relatedness in strains of Acidithiobacillus ferrooxidans . J Microbiol Methods 62:103–112
    [Google Scholar]
  69. Wayne L. G., Brenner D. J., Colwell R. R., Grimont P. A. D., Kandler O., Krichevsky M. I., Moore L. H., Moore W. E. C., Murray R. G. E., other authors A. E. 1987; International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464
    [Google Scholar]
  70. Williams K. P., Gillespie J. J., Sobral B. W., Nordberg E. K., Snyder E. E., Shallom J. M., Dickerman A. W. 2010; Phylogeny of gammaproteobacteria. J Bacteriol 192:2305–2314
    [Google Scholar]
  71. Yarzábal A., Duquesne K., Bonnefoy V. 2003; Rusticyanin gene expression of Acidithiobacillus ferrooxidans ATCC 33020 in sulfur- and in ferrous iron-media. Hydrometallurgy 71:107–114
    [Google Scholar]
  72. 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
    [Google Scholar]
  73. Young J. M., Park D. C., Shearman H. M., Fargier E. 2008; A multilocus sequence analysis of the genus Xanthomonas . Syst Appl Microbiol 31:366–377
    [Google Scholar]
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