1887

Abstract

Acidophilic micro-organisms inhabit some of the most metal-rich environments known, including both natural and man-made ecosystems, and as such are ideal model systems for study of microbial metal resistance. Although metal resistance systems have been studied in neutrophilic micro-organisms, it is only in recent years that attention has been placed on metal resistance in acidophiles. The five metal resistance mechanisms identified in neutrophiles are also present in acidophiles, in some cases utilizing homologous proteins, but in many cases the degree of resistance is greater in acidophiles. This review summarizes the knowledge of acidophile metal resistance and presents preliminary studies on a few known metal resistance systems in the sequenced acidophile genomes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26296-0
2003-08-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/8/mic1491959.html?itemId=/content/journal/micro/10.1099/mic.0.26296-0&mimeType=html&fmt=ahah

References

  1. Baillet, F., Magnin, J. P., Cheruy, A. & Ozil, P. ( 1997; ). Cadmium tolerance and uptake in Thiobacillus ferrooxidans biomass. Environ Technol 18, 631–637.[CrossRef]
    [Google Scholar]
  2. Baillet, F., Magnin, J. P., Cheruy, A. & Ozil, P. ( 1998; ). Chromium precipitation by the acidophilic bacterium Thiobacillus ferrooxidans. Biotechnol Lett 20, 95–99.[CrossRef]
    [Google Scholar]
  3. Bond, P. L., Smriga, S. P. & Banfield, J. F. ( 2000a; ). Phylogeny of microorganisms populating a thick, subaerial, predominantly lithotrophic biofilm at an extreme acid mine drainage site. Appl Environ Microbiol 66, 3842–3849.[CrossRef]
    [Google Scholar]
  4. Bond, P. L., Druschel, G. K. & Banfield, J. F. ( 2000b; ). Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems. Appl Environ Microbiol 66, 4962–4971.[CrossRef]
    [Google Scholar]
  5. Boon, M., Ras, C. & Heijnen, J. J. ( 1999a; ). The ferrous iron oxidation kinetics of Thiobacillus ferrooxidans in batch cultures. Appl Microbiol Biotechnol 51, 813–819.[CrossRef]
    [Google Scholar]
  6. Boon, M., Meeder, T. A., Thione, C., Ras, C. & Heijnen, J. J. ( 1999b; ). The ferrous iron oxidation kinetics of Thiobacillus ferrooxidans in continuous culture. Appl Microbiol Biotechnol 51, 820–826.[CrossRef]
    [Google Scholar]
  7. Booth, J. E. & Williams, J. W. ( 1984; ). The isolation of a mercuric ion-reducing flavoprotein from Thiobacillus ferrooxidans. J Gen Microbiol 130, 725–730.
    [Google Scholar]
  8. Boyer, A., Magnin, J. P. & Ozil, P. ( 1998; ). Copper ion removal by Thiobacillus ferrooxidans biomass. Biotechnol Lett 20, 187–190.[CrossRef]
    [Google Scholar]
  9. Bruins, M. R., Kapil, S. & Oehme, F. W. ( 2000; ). Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45, 198–207.[CrossRef]
    [Google Scholar]
  10. Burton, N. P. & Norris, P. R. ( 2000; ). Microbiology of acidic, geothermal springs of Montserrat: environmental rDNA analysis. Extremophiles 4, 315–320.[CrossRef]
    [Google Scholar]
  11. Butcher, B. G. & Rawlings, D. E. ( 2002; ). The divergent chromosomal ars operon of Acidithiobacillus ferrooxidans is regulated by an atypical ArsR protein. Microbiology 148, 3983–3992.
    [Google Scholar]
  12. Butcher, B. G., Shelly, M. D. & Rawlings, D. E. ( 2000; ). The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66, 1826–1833.[CrossRef]
    [Google Scholar]
  13. Carlin, A., Shi, W., Dey, S. & Rosen, B. P. ( 1995; ). The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177, 981–986.
    [Google Scholar]
  14. Cerruti, C., Curutchet, G. & Donati, E. ( 1998; ). Bio-dissolution of spent nickel-cadmium batteries using Thiobacillus ferrooxidans. J Biotechnol 62, 209–219.[CrossRef]
    [Google Scholar]
  15. Chisholm, I. A., Leduc, L. G. & Ferroni, G. D. ( 1998; ). Metal resistance and plasmid DNA in Thiobacillus ferrooxidans. Antonie van Leeuwenhoek 73, 245–254.[CrossRef]
    [Google Scholar]
  16. Clark, D. A. & Norris, P. R. ( 1996; ). Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142, 785–790.[CrossRef]
    [Google Scholar]
  17. Curutchet, G., Pogliani, C., Donati, E. & Tedesco, P. ( 1992; ). Effect of iron (III) and its hydrolysis products (jarosites) on Thiobacillus ferrooxidans growth and on bacterial leaching. Biotechnol Lett 14, 329–334.[CrossRef]
    [Google Scholar]
  18. Das, A., Modak, J. M. & Natarajan, K. A. ( 1997; ). Studies on multi-metal ion tolerance of Thiobacillus ferrooxidans. Miner Eng 10, 743–749.[CrossRef]
    [Google Scholar]
  19. Das, A., Modak, J. M. & Natarajan, K. A. ( 1998; ). Surface chemical studies of Thiobacillus ferrooxidans with reference to copper tolerance. Antonie van Leeuwenhoek 73, 215–222.[CrossRef]
    [Google Scholar]
  20. De, G. C., Oliver, D. J. & Pesic, B. M. ( 1996; ). Effect of silver on the ferrous iron oxidizing ability of Thiobacillus ferrooxidans. Hydrometallurgy 41, 211–229.[CrossRef]
    [Google Scholar]
  21. De, G. C., Oliver, D. J. & Pesic, B. M. ( 1997; ). Effect of heavy metals on the ferrous iron oxidizing ability of Thiobacillus ferrooxidans. Hydrometallurgy 44, 53–63.[CrossRef]
    [Google Scholar]
  22. de Groot, P., Deane, S. M. & Rawlings, D. E. ( 2001; ). A transposon-located arsenic resistance mechanism within the chromosome of the biomining bacterium, Acidithiobacillus caldus. In International Biohydrometallurgy Symposium, pp. 271–281. Edited by V. S. T. Ciminelli & O. Garcia, Jr. Ouro Preto, Brazil: Elsevier.
  23. Dew, D. W., Muhlbauer, R. & van Buuren, C. ( 1999; ). Bioleaching of copper sulphide concentrates with mesophiles and thermophiles. In Alta Copper 99. Brisbane, Australia.
  24. De Wulf-Durand, P., Bryant, L. J. & Sly, L. I. ( 1997; ). PCR-mediated detection of acidophilic, bioleaching-associated bacteria. Appl Environ Microbiol 63, 2944–2948.
    [Google Scholar]
  25. Dispiroto, A. A., Talnagi, J. W. & Tuovinen, O. H. ( 1983; ). Accumulation and cellular-distribution of uranium in Thiobacillus ferrooxidans. Arch Microbiol 135, 250–253.[CrossRef]
    [Google Scholar]
  26. Dopson, M., Lindström, E. B. & Hallberg, K. B. ( 2001; ). Chromosomally encoded arsenical resistance of the moderately thermophilic acidophile Acidithiobacillus caldus. Extremophiles 5, 247–255.[CrossRef]
    [Google Scholar]
  27. Ehrlich, H. L. ( 1984; ). Growth of Thiobacillus ferrooxidans in the presence of silver compounds. In Abstracts of the 84th Annual Meeting of the American Society for Microbiology, St Louis, Missouri, USA, 1984, p. 197, abstract O50. Washington, DC: American Society for Microbiology.
  28. Espejo, R. T. & Romero, J. ( 1997; ). Bacterial community in copper sulfide ores inoculated and leached with solution from a commercial-scale copper leaching plant. Appl Environ Microbiol 63, 1344–1348.
    [Google Scholar]
  29. Ghosh, S., Mahapatra, N. R. & Banerjee, P. C. ( 1997; ). Metal resistance in Acidocella strains and plasmid-mediated transfer of this characteristic to Acidiphilium multivorum and Escherichia coli. Appl Environ Microbiol 63, 4523–4527.
    [Google Scholar]
  30. Ghosh, S., Mahapatra, N. R., Ramamurthy, T. & Banerjee, P. C. ( 2000; ). Plasmid curing from an acidophilic bacterium of the genus Acidocella. FEMS Microbiol Lett 183, 271–274.[CrossRef]
    [Google Scholar]
  31. Gihring, T. M., Bond, P. L., Peters, S. C. & Banfield, J. F. ( 2003; ). Arsenic resistance in the archaeon Ferroplasma acidarmanus: new insights into the structure and evolution of the ars genes. Extremophiles 7, 123–130.
    [Google Scholar]
  32. Goebel, B. M. & Stackebrandt, E. ( 1994; ). Cultural and phylogenetical analysis of mixed microbial populations found in natural and commercial bioleaching environments. Appl Environ Microbiol 60, 1614–1621.
    [Google Scholar]
  33. Gomez, E., Ballester, A., Gonzalez, F. & Blazquez, M. L. ( 1999; ). Leaching capacity of a new extremely thermophilic microorganism, Sulfolobus rivotincti. Hydrometallurgy 52, 349–366.[CrossRef]
    [Google Scholar]
  34. Grundy, W. N., Bailey, T. L., Elkan, C. P. & Baker, M. E. ( 1997; ). Meta-meme: motif-based hidden Markov models of protein families. Comput Appl Biosci 13, 397–406.
    [Google Scholar]
  35. Guay, R., Ghosh, J. & Torma, A. E. ( 1989; ). Kinetics of microbiological production of ferric ion for heap and dump leaching. In Biotechnology in Minerals and Metals Processing, pp. 95–106. Edited by B. J. Scheiner, F. M. Doyle & S. K. Kawatra. Littleton, CO: Society of Mining Engineers.
  36. Hallberg, K. B. ( 1995; ). Role of arsenic toxicity to and arsenic resistance of thermophilic bioleaching microorganisms. Thesis. Department of Applied Cell and Molecular Biology, Umeå University.
  37. Hallberg, K. B. & Johnson, D. B. ( 2001; ). Biodiversity of acidophilic prokaryotes. Adv Appl Microbiol 49, 37–84.
    [Google Scholar]
  38. Hallberg, K. B., Dopson, M. & Lindström, E. B. ( 1996; ). Arsenic toxicity is not due to a direct effect on the oxidation of reduced sulfur compounds by Thiobacillus caldus. FEMS Microbiol Lett 145, 409–414.[CrossRef]
    [Google Scholar]
  39. Harvey, P. I. & Crundwell, F. K. ( 1996; ). The effect of As(III) on the growth of Thiobacillus ferrooxidans in an electrolytic cell under controlled redox potential. Min Eng 9, 1059–1068.[CrossRef]
    [Google Scholar]
  40. Huber, G., Spinnler, C., Gambacorta, A. & Stetter, K. O. ( 1989; ). Metallosphaera sedula gen. and sp. nov. represents a new genus of aerobic, metal-mobilizing, thermoacidophilic archaebacteria. Syst Appl Microbiol 12, 38–47.[CrossRef]
    [Google Scholar]
  41. Imai, K., Sugio, T., Tsuchida, T. & Tano, T. ( 1975; ). Effect of heavy metal ions on growth and iron-oxidizing activity of Thiobacillus ferrooxidans. Agric Biol Chem 39, 1349–1354.[CrossRef]
    [Google Scholar]
  42. Inoue, C., Sugawara, K. & Kusano, T. ( 1991; ). The merR regulatory gene in Thiobacillus ferrooxidans is spaced apart from the mer structural genes. Mol Microbiol 5, 2707–2718.[CrossRef]
    [Google Scholar]
  43. Itoh, S., Iwaka, M., Wakao, N., Yoshizu, K., Aoki, A. & Tazaki, K. ( 1998; ). Accumulation of Fe, Cr and Ni metals inside cells of acidophilic bacterium Acidiphilum rubrum that produces Zn-containing bacteriochlorophyll a. Plant Cell Physiol 39, 740–744.[CrossRef]
    [Google Scholar]
  44. Johnson, D. B., Ghauri, M. A. & Said, M. F. ( 1992; ). Isolation and characterization of an acidophilic, heterotrophic bacterium capable of oxidizing ferrous iron. Appl Environ Microbiol 58, 1423–1428.
    [Google Scholar]
  45. Kalyaeva, E. S., Kholodii, G. Y., Bass, I. A., Gorlenko, Z. M., Yureiva, O. V. & Nikiforov, V. G. ( 2001; ). Tn5037, a Tn21-like mercury resistance transposon from Thiobacillus ferrooxidans. Russ J Genet 37, 972–975.[CrossRef]
    [Google Scholar]
  46. Karamanev, D. G. & Nikolov, L. N. ( 1988; ). Influence of some physiochemical parameters on bacterial activity of biofilm: ferrous iron oxidation by Thiobacillus ferrooxidans. Biotechnol Bioeng 31, 295–299.[CrossRef]
    [Google Scholar]
  47. Kondratyeva, T. F., Muntyan, L. N. & Karavaiko, G. I. ( 1995; ). Zinc- and arsenic-resistant strains of Thiobacillus ferrooxidans have increased copy numbers of chromosomal resistance genes. Microbiology 141, 1157–1162.[CrossRef]
    [Google Scholar]
  48. LaPlagia, C. & Hartzell, P. L. ( 1997; ). Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus. Appl Environ Microbiol 63, 3158–3163.
    [Google Scholar]
  49. Ledin, M. & Pedersen, K. ( 1996; ). The environmental impact of mine wastes – roles of microorganisms and their significance in treatment of mine wastes. Earth-Sci Rev 41, 67–108.[CrossRef]
    [Google Scholar]
  50. Maeda, T., Negishi, A., Nogami, Y. & Sugio, T. ( 1996; ). Nickel inhibition of the growth of a sulfur-oxidizing bacterium isolated from corroded concrete. Biosci Biotechnol Biochem 60, 626–629.[CrossRef]
    [Google Scholar]
  51. Mahapatra, N. R. & Banerjee, P. C. ( 1996; ). Extreme tolerance to cadmium and high resistance to copper, nickel and zinc in different Acidiphilium strains. Lett Appl Microbiol 23, 393–397.[CrossRef]
    [Google Scholar]
  52. Mahapatra, N. R., Ghosh, S., Deb, C. & Banerjee, P. C. ( 2002; ). Resistance to cadmium and zinc in Acidiphilium symbioticum KM2 is plasmid mediated. Curr Microbiol 45, 180–186.[CrossRef]
    [Google Scholar]
  53. Mier, J. L., Ballester, A., Gonzalez, F., Blazquez, M. L. & Gomez, E. ( 1996; ). The influence of metallic ions on the activity of Sulfolobus BC. J Chem Technol Biotechnol 65, 272–280.[CrossRef]
    [Google Scholar]
  54. Miller, K. W., Risanico, S. S. & Risatti, J. B. ( 1992; ). Differential tolerance of Sulfolobus strains to transition-metals. FEMS Microbiol Lett 93, 69–73.[CrossRef]
    [Google Scholar]
  55. Miller, P. C., Rhodes, M. K., Winby, R., Pinches, A. & van Staden, P. J. ( 1999; ). Commercialization of bioleaching for base-metal extraction. Miner Metallurg Process 16, 42–50.
    [Google Scholar]
  56. Nies, D. H. ( 1999; ). Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51, 730–750.[CrossRef]
    [Google Scholar]
  57. Nogami, Y., Maeda, T., Negishi, A. & Sugio, T. ( 1997; ). Inhibition of sulfur oxidizing activity by nickel ion in Thiobacillus ferrooxidans NB1-3 isolated from the corroded concrete. Biosci Biotechnol Biochem 61, 1373–1375.[CrossRef]
    [Google Scholar]
  58. Nordstrom, D. K. & Alpers, C. N. ( 1999; ). Negative pH, efflorescent mineralogy, and consequences for environmental restoration at the iron mountain superfund site, California. Proc Natl Acad Sci U S A 96, 3455–3462.[CrossRef]
    [Google Scholar]
  59. Norris, P. R. & Kelly, D. P. ( 1978; ). Toxic metals in leaching systems. In Metallurgical Applications of Bacterial Leaching and Related Microbiological Phenomena, pp. 85–102. Edited by L. E. Murr, A. E. Torma & J. A. Brierley. New York & London: Academic Press.
  60. Novo, M. T., da Silva, A. C., Moreto, R., Cabral, P. C., Costacurta, A., Garcia, O., Jr & Ottoboni, L. M. ( 2000; ). Thiobacillus ferrooxidans response to copper and other heavy metals: growth, protein synthesis and protein phosphorylation. Antonie van Leeuwenhoek 77, 187–195.[CrossRef]
    [Google Scholar]
  61. Olson, G. J., Porter, F. D., Rubenstein, J. & Silver, S. ( 1982; ). Mercuric reductase enzyme from a mercury-volatilizing strain of Thiobacillus ferrooxidans. J Bacteriol 151, 1230–1236.
    [Google Scholar]
  62. Osborn, A. M., Bruce, K. D., Strike, P. & Ritchie, D. A. ( 1997; ). Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol Rev 19, 239–262.[CrossRef]
    [Google Scholar]
  63. Paulino, L. C., de Mello, M. P. & Ottoboni, L. M. ( 2002; ). Differential gene expression in response to copper in Acidithiobacillus ferrooxidans analyzed by RNA arbitrarily primed polymerase chain reaction. Electrophoresis 23, 520–527.[CrossRef]
    [Google Scholar]
  64. Pooley, F. D. ( 1982; ). Bacteria accumulate silver during leaching of sulfide ore minerals. Nature 296, 642–643.[CrossRef]
    [Google Scholar]
  65. Pramila, T., Ramananda, R., Natarajan, K. A. & Durga Rao, C. ( 1996; ). Differential influence of ions on the copy number of plasmids in Thiobacillus ferrooxidans. Curr Microbiol 32, 57–63.[CrossRef]
    [Google Scholar]
  66. Rawlings, D. E., Tributsch, H. & Hansford, G. S. ( 1999; ). Reasons why ‘Leptospirillum’-like species rather than Thiobacillus ferrooxidans are the dominant iron-oxidizing bacteria in many commercial processes for the biooxidation of pyrite and related ores. Microbiology 145, 5–13.[CrossRef]
    [Google Scholar]
  67. Rondon, M. R., August, P. R., Bettermann, A. D. & 13 other authors ( 2000; ). Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 66, 2541–2547.[CrossRef]
    [Google Scholar]
  68. Ruepp, A., Graml, W., Santos-Martinez, M. L. & 7 other authors ( 2000; ). The genome sequence of the thermoacidophilic scavenger Thermoplasma acidophilum. Nature 407, 508–513.[CrossRef]
    [Google Scholar]
  69. Sampson, M. I. & Phillips, C. V. ( 2001; ). Influence of base metals on the oxidising ability of acidophilic bacteria during the oxidation of ferrous sulfate and mineral sulfide concentrates, using mesophiles and moderate thermophiles. Miner Eng 14, 317–340.[CrossRef]
    [Google Scholar]
  70. Sehlin, H. M. & Lindström, E. B. ( 1992; ). Oxidation and reduction of arsenic by Sulfolobus acidocaldarius strain BC. FEMS Microbiol Lett 93, 87–92.[CrossRef]
    [Google Scholar]
  71. Shrihari, R. K. & Gandhi, K. S. ( 1990; ). Modelling of Fe2+ oxidation by Thiobacillus ferrooxidans. Appl Microbiol Biotechnol 33, 524–528.
    [Google Scholar]
  72. Sugio, T., Iwahori, K., Takeuchi, F., Negishi, A., Maeda, T. & Kamimura, K. ( 2001; ). Cytochrome c oxidase purified from a mercury-resistant strain of Acidithiobacillus ferrooxidans volatizes mercury. J Biosci Bioeng 92, 44–49.[CrossRef]
    [Google Scholar]
  73. Suzuki, K., Wakao, N., Sakurai, Y., Kimura, T., Sakka, K. & Ohmiya, K. ( 1997; ). Transformation of Escherichia coli with a large plasmid of Acidiphilium multivorum AIU 301 encoding arsenic resistance. Appl Environ Microbiol 63, 2089–2091.
    [Google Scholar]
  74. Suzuki, K., Wakao, N., Kimura, T., Sakka, K. & Ohmiya, K. ( 1998; ). Expression and regulation of the arsenic resistance operon of Acidiphilium multivorum AIU 301 plasmid pKW301 in Escherichia coli. Appl Environ Microbiol 64, 411–418.
    [Google Scholar]
  75. Takeuchi, F., Iwahori, K., Kamimura, K. & Sugio, T. ( 1999; ). Isolation and some properties of Thiobacillus ferrooxidans strains with differing levels of mercury resistance from natural environments. J Biosci Bioeng 88, 387–392.[CrossRef]
    [Google Scholar]
  76. Takeuchi, F., Iwahori, K., Kamimura, K., Negishi, A., Maeda, T. & Sugio, T. ( 2001; ). Volatilization of mercury under acidic conditions from mercury-polluted soil by a mercury-resistant Acidithiobacillus ferrooxidans SUG 2-2. Biosci Biotechnol Biochem 65, 1981–1986.[CrossRef]
    [Google Scholar]
  77. Trevors, J. T., Oddie, K. M. & Belliveau, B. H. ( 1985; ). Metal resistance in bacteria. FEMS Microbiol Rev 32, 39–54.[CrossRef]
    [Google Scholar]
  78. Tuovinen, O. H. & Bhatti, T. M. ( 1999; ). Microbiological leaching of uranium ores. Miner Metallurg Process 16, 51–60.
    [Google Scholar]
  79. van Scherpenzel, D. A., Boon, M., Ras, C., Hansford, G. S. & Heijnen, J. J. ( 1988; ). Kinetics of ferrous iron oxidation by Leptospirillium bacteria in continuous culture. Biotechnol Prog 14, 425–433.
    [Google Scholar]
  80. Vartanyan, N. S., Karavaiko, G. I., Pivovarova, T. A. & Dorofeev, A. G. ( 1990; ). Resistance of Sulfobacillus thermosulfidooxidans subspecies asporogenes to Cu2+, Zn2+ and Ni2+ ions. Microbiology (English translation of Mikrobiologiya) 59, 399–404.
    [Google Scholar]
  81. Velasco, A., Acebo, P., Flores, N. & Perera, J. ( 1999; ). The mer operon of the acidophilic bacterium Thiobacillus T3.2 diverges from its Thiobacillus ferrooxidans counterpart. Extremophiles 3, 35–43.[CrossRef]
    [Google Scholar]
  82. Wong, C., Silver, M. & Kushner, D. J. ( 1982; ). Effects of chromium and manganese on Thiobacillus ferrooxidans. Can J Microbiol 28, 536–544.[CrossRef]
    [Google Scholar]
  83. Xu, C., Zhou, T., Kuroda, M. & Rosen, B. P. ( 1998; ). Metalloid resistance mechanisms in prokaryotes. J Biochem (Tokyo) 123, 16–23.[CrossRef]
    [Google Scholar]
  84. Yong, N. K., Oshima, M., Blake, R. C. & Sugio, T. ( 1997; ). Isolation and some properties of an iron-oxidizing bacterium Thiobacillus ferrooxidans resistant to molybdenum ion. Biosci Biotechnol Biochem 61, 1523–1526.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26296-0
Loading
/content/journal/micro/10.1099/mic.0.26296-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error