Table of Contents Author Guidelines Submit a Manuscript
The Scientific World Journal
Volume 2015, Article ID 761834, 14 pages
http://dx.doi.org/10.1155/2015/761834
Research Article

Resistance to and Accumulation of Heavy Metals by Actinobacteria Isolated from Abandoned Mining Areas

1Environmental Microbiology and Toxicology Unit, Laboratory of Biology and Biotechnology of Microorganisms (LBBM), Faculty of Sciences Semlalia, Cadi Ayyad University, P.O. Box 2390, 40000 Marrakech, Morocco
2Laboratory of Hydrobiology, Ecotoxicology and Assainissement (LHEA), Faculty of Sciences Semlalia, Cadi Ayyad University, P.O. Box 2390, 40000 Marrakech, Morocco

Received 7 August 2014; Revised 13 November 2014; Accepted 18 November 2014

Academic Editor: Wen-Jun Li

Copyright © 2015 Soraia El Baz et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Valdman, L. Erijman, F. L. P. Pessoa, and S. G. F. Leite, “Continuous biosorption of Cu and Zn by immobilized waste biomass Sargassum sp,” Process Biochemistry, vol. 36, no. 8-9, pp. 869–873, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. I. H. Çeribasi and U. Yetis, “Biosorption of Ni(ii) and Pb(ii) by Phanerochaete chrysosporium from a binary metal system—kinetics,” Water SA, vol. 27, no. 1, pp. 15–20, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Zafar, F. Aqil, and I. Ahmad, “Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil,” Bioresource Technology, vol. 98, no. 13, pp. 2557–2561, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Haferburg and E. Kothe, “Microbes and metals: interactions in the environment,” Journal of Basic Microbiology, vol. 47, no. 6, pp. 453–467, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Ezzouhri, E. Castro, M. Moya, F. Espinola, and K. Lairini, “Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier, Morocco,” African Journal of Microbiology Research, vol. 3, no. 2, pp. 35–48, 2009. View at Google Scholar
  6. M. R. Bruins, S. Kapil, and F. W. Oehme, “Microbial resistance to metals in the environment,” Ecotoxicology and Environmental Safety, vol. 45, no. 3, pp. 198–207, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Selvin, S. Shanmugha Priya, G. Seghal Kiran, T. Thangavelu, and N. Sapna Bai, “Sponge-associated marine bacteria as indicators of heavy metal pollution,” Microbiological Research, vol. 164, no. 3, pp. 352–363, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Zapotoczny, A. Jurkiewicz, G. Tylko, T. Anielska, and K. Turnau, “Accumulation of copper by Acremonium pinkertoniae, a fungus isolated from industrial wastes,” Microbiological Research, vol. 162, no. 3, pp. 219–228, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. V. N. Kavamura and E. Esposito, “Biotechnological strategies applied to the decontamination of soils polluted with heavy metals,” Biotechnology Advances, vol. 28, no. 1, pp. 61–69, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Solecka, J. Zajko, M. Postek, and A. Rajnisz, “Biologically active secondary metabolites from Actinomycetes,” Central European Journal of Biology, vol. 7, no. 3, pp. 373–390, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. M. S. Louis, J. M. Benito, V. H. Albarracín, T. Lebeau, M. J. Amoroso, and C. M. Abate, “Heavy-metal resistant actinomycetes,” in Heavy-Metal Resistant Actinomycetes, E. Lichtfouse, J. Schwarzbauer, and D. Robert, Eds., pp. 757–767, Springer, Berlin, Germany, 2005. View at Google Scholar
  12. J. Bérdy, “Bioactive microbial metabolites,” The Journal of Antibiotics, vol. 58, no. 1, pp. 1–26, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Schmidt, G. Haferburg, M. Sineriz, D. Merten, G. Büchel, and E. Kothe, “Heavy metal resistance mechanisms in actinobacteria for survival in AMD contaminated soils,” Chemie der Erde—Geochemistry, vol. 65, Supplement 1, pp. 131–144, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. N.-W. So, J.-Y. Rho, S.-Y. Lee, I. C. Hancock, and J.-H. Kim, “A lead-absorbing protein with superoxide dismutase activity from Streptomyces subrutilus,” FEMS Microbiology Letters, vol. 194, no. 1, pp. 93–98, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. V. L. Colin, L. B. Villegas, and C. M. Abate, “Indigenous microorganisms as potential bioremediators for environments contaminated with heavy metals,” International Biodeterioration & Biodegradation, vol. 69, pp. 28–37, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. M. A. Polti, M. J. Amoroso, and C. M. Abate, “Chromium(VI) resistance and removal by actinomycete strains isolated from sediments,” Chemosphere, vol. 67, no. 4, pp. 660–667, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. V. H. Albarracín, P. Alonso-Vega, M. E. Trujillo, M. J. Amoroso, and C. M. Abate, “Amycolatopsis tucumanensis sp. nov., a copper-resistant actinobacterium isolated from polluted sediments,” International Journal of Systematic and Evolutionary Microbiology, vol. 60, part 2, pp. 397–401, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. V. H. Albarracín, B. Winik, E. Kothe, M. J. Amoroso, and C. M. Abate, “Copper bioaccumulation by the actinobacterium Amycolatopsis sp. AB0,” Journal of Basic Microbiology, vol. 48, no. 5, pp. 323–330, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. J. S. D. Costa, V. H. Albarracín, and C. M. Abate, “Responses of environmental Amycolatopsis strains to copper stress,” Ecotoxicology and Environmental Safety, vol. 74, no. 7, pp. 2020–2028, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. M. S. Fuentes, C. S. Benimeli, S. A. Cuozzo, and M. J. Amoroso, “Isolation of pesticide-degrading actinomycetes from a contaminated site: bacterial growth, removal and dechlorination of organochlorine pesticides,” International Biodeterioration and Biodegradation, vol. 64, no. 6, pp. 434–441, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. A. EL Gharmali, Impact des résidus miniers et des eaux résiduaires sur la contamination métallique des écosystèmes aquatiques et terrestres de la région de Marrakech, Maroc [Ph.D. thesis], University Cadi Ayyad, Marrakech, Morocco, 2005.
  22. M. Hakkou, M. Pétrissans, I. El Bakali, P. Gérardin, and A. Zoulalian, “Wettability changes and mass loss during heat treatment of wood,” Holzforschung, vol. 59, no. 1, pp. 35–37, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. AFNOR, Quality of Soil. Soils, Sediments, Mise en Solution Totale par Attaque Acide, AFNOR, Paris, France, 1996.
  24. G. Aubert, Methods of Soil Analysis, G.R.D.P., Marseille, France, 1978.
  25. K. L. Jones, “Fresh isolates of actinomycetes in which the presence of sporogenous,” Journal of Bacteriology, vol. 57, no. 2, pp. 141–145, 1949. View at Google Scholar · View at Scopus
  26. T. Duxbury, “Toxicity of heavy metals to soil bacteria,” FEMS Microbiology Letters, vol. 11, no. 2-3, pp. 217–220, 1981. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Hernández, R. P. Mellado, and J. L. Martínez, “Metal accumulation and vanadium-induced multidrug resistance by environmental isolates of Escherichia hermannii and Enterobacter cloacae,” Applied and Environmental Microbiology, vol. 64, no. 11, pp. 4317–4320, 1998. View at Google Scholar · View at Scopus
  28. E. B. Shirling and D. Gottlieb, “Methods for characterization of streptomyces species,” International Journal of Systematic Bacteriology, vol. 16, no. 3, pp. 313–340, 1966. View at Google Scholar
  29. H. Prauser, “Aptness and application of colour codes for exact description of colours of Streptomycetes,” Zeitschrift für Allgemeine Mikrobiologie, vol. 4, no. 1, pp. 95–98, 1964. View at Publisher · View at Google Scholar · View at Scopus
  30. D. A. Hopwood, M. J. Bibb, K. F. Chater et al., Genetic Manipulation of Streptomyces. A Laboratory Manual, The John Innes Institute, Norwich, UK, 1985.
  31. D. J. Lane, “16S/23S rRNA sequencing,” in Nucleic Acid Techniques in Bacterial Systematics, E. Stackebrandt and M. Goodfellow, Eds., pp. 115–175, John Wiley & Sons, New York, NY, USA, 1991. View at Google Scholar
  32. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar, “MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2731–2739, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. B. Schwyn and J. B. Neilands, “Universal chemical assay for the detection and determination of siderophores,” Analytical Biochemistry, vol. 160, no. 1, pp. 47–56, 1987. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Z. Csaky, “On the estimation of bound hydroxylamine in biological materials,” Acta Chemica Scandinavica, vol. 2, pp. 450–454, 1948. View at Publisher · View at Google Scholar
  35. L. E. Arnow, “Colorimetric determination of the components of 3, 4-dihydroxyphenylalanine—tyrosine mixtures,” The Journal of Biological Chemistry, vol. 118, pp. 531–537, 1937. View at Google Scholar
  36. J. B. Neilands and K. Nakamura, “Detection, determination, isolation, characterization and regulation of microbial iron chelates,” in CRC Handbook of Microbial Iron Chelates, G. Winkelmann, Ed., pp. 1–14, CRC Press, Boca Raton, Fla, USA, 1991. View at Google Scholar
  37. H. Holmström, J. Ljungberg, and B. Öhlander, “The character of the suspended and dissolved phases in the water cover of the flooded mine tailings at Stekenjokk, Northern Sweden,” Science of the Total Environment, vol. 247, no. 1, pp. 15–31, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Holmström and B. Öhlander, “Layers rich in Fe- and Mn-oxyhydroxides formed at the tailings-pond water interface, a possible trap for trace metals in flooded mine tailings,” Journal of Geochemical Exploration, vol. 74, no. 1–3, pp. 189–203, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Ljungberg and B. Öhlander, “The geochemical dynamics of oxidising mine tailings at Laver, Northern Sweden,” Journal of Geochemical Exploration, vol. 74, no. 1–3, pp. 57–72, 2001. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Vigneault, P. G. C. Campbell, A. Tessier, and R. de Vitre, “Geochemical changes in sulfidic mine tailings stored under a shallow water cover,” Water Research, vol. 35, no. 4, pp. 1066–1076, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. S. R. Jennings, D. J. Dollhopf, and W. P. Inskeep, “Acid production from sulfide minerals using hydrogen peroxide weathering,” Applied Geochemistry, vol. 15, no. 2, pp. 235–243, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Khalil, L. Hanich, R. Hakkou, and M. Lepage, “GIS-based environmental database for assessing the mine pollution: a case study of an abandoned mine site in Morocco,” Journal of Geochemical Exploration, vol. 144, part C, pp. 468–477, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Lghoul, A. Maqsoud, R. Hakkou, and A. Kchikach, “Hydrogeochemical behavior around the abandoned Kettara mine site, Morocco,” Journal of Geochemical Exploration, vol. 144, part C, pp. 456–467, 2013. View at Publisher · View at Google Scholar
  44. R. S. Laxman and S. More, “Reduction of hexavalent chromium by Streptomyces griseus,” Minerals Engineering, vol. 15, no. 11, pp. 831–837, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. P. Majzlik, A. Strasky, V. Adam et al., “Influence of zinc(II) and copper(II) ions on Streptomyces bacteria revealed by electrochemistry,” International Journal of Electrochemical Science, vol. 6, no. 6, pp. 2171–2191, 2011. View at Google Scholar · View at Scopus
  46. A. Schmidt, G. Haferburg, U. Lischke et al., “Heavy metal resistance to the extreme: streptomyces strains from a former uranium mining area,” Chemie der Erde—Geochemistry, vol. 69, supplement 2, pp. 35–44, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. J. G. Holt, N. R. Krieg, P. H. A. Sneath, J. T. Staley, and S. T. Williams, Bergey’s Manual of Determinative Bacteriology, Williams & Williams, Baltimore, Md, USA, 9th edition, 1994.
  48. E. Stackebrandt, F. A. Rainey, and N. L. Ward-Rainey, “Proposal for a new hierarchic classification system, Actinobacteria classis nov,” International Journal of Systematic Bacteriology, vol. 47, no. 2, pp. 479–491, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Aleem, J. Isar, and A. Malik, “Impact of long-term application of industrial wastewater on the emergence of resistance traits in Azotobacter chroococcum isolated from rhizospheric soil,” Bioresource Technology, vol. 86, no. 1, pp. 7–13, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Sanjenbam, K. Saurav, and K. Kannabiran, “Biosorption of mercury and lead by aqueous Streptomyces VITSVK9 sp. isolated from marine sediments from the bay of Bengal, India,” Frontiers of Chemical Science and Engineering, vol. 6, no. 2, pp. 198–202, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. V. H. Albarracín, M. J. Amoroso, and C. M. Abate, “Isolation and characterization of indigenous copper-resistant actinomycete strains,” Chemie der Erde—Geochemistry, vol. 65, Supplement 1, pp. 145–156, 2005. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Ge, P. Murray, and W. H. Hendershot, “Trace metal speciation and bioavailability in urban soils,” Environmental Pollution, vol. 107, no. 1, pp. 137–144, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. C. E. Martínez and H. L. Motto, “Solubility of lead, zinc and copper added to mineral soils,” Environmental Pollution, vol. 107, no. 1, pp. 153–158, 2000. View at Publisher · View at Google Scholar · View at Scopus
  54. G. M. Gadd, “Metals and microorganisms: a problem of definition,” FEMS Microbiology Letters, vol. 100, no. 1–3, pp. 197–203, 1992. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Y. Rho and J. H. Kim, “Heavy metal biosorption and its significance to metal tolerance of streptomycetes,” The Journal of Microbiology, vol. 40, no. 1, pp. 51–54, 2002. View at Google Scholar
  56. W. Lo, H. Chua, K.-H. Lam, and S.-P. Bi, “A comparative investigation on the biosorption of lead by filamentous fungal biomass,” Chemosphere, vol. 39, no. 15, pp. 2723–2736, 1999. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Słaba and J. Długoński, “Zinc and lead uptake by mycelium and regenerating protoplasts of Verticillium marquandii,” World Journal of Microbiology and Biotechnology, vol. 20, no. 3, pp. 323–328, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Mattuschka, G. Straube, and J. T. Trevors, “Silver, copper, lead and zinc accumulation by Pseudomonas stutzeri AG259 and Streptomyces albus: electron microscopy and energy dispersive X-ray studies,” BioMetals, vol. 7, no. 2, pp. 201–208, 1994. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Lin, X. Wang, B. Wang, O. Mohamad, and G. Wei, “Bioaccumulation characterization of zinc and cadmium by Streptomyces zinciresistens, a novel actinomycete,” Ecotoxicology and Environmental Safety, vol. 77, pp. 7–17, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. I. Nakouti and G. Hobbs, “A new approach to studying ion uptake by actinomycetes,” Journal of Basic Microbiology, vol. 53, no. 11, pp. 913–916, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. W. Wang, Z. Qiu, H. Tan, and L. Cao, “Siderophore production by actinobacteria,” BioMetals, vol. 27, no. 4, pp. 623–631, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Gaonkar and S. Bhosle, “Effect of metals on a siderophore producing bacterial isolate and its implications on microbial assisted bioremediation of metal contaminated soils,” Chemosphere, vol. 93, no. 9, pp. 1835–1843, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Álvarez, S. A. Catalano, and M. J. Amoroso, “Heavy metal resistant strains are widespread along Streptomyces phylogeny,” Molecular Phylogenetics and Evolution, vol. 66, no. 3, pp. 1083–1088, 2013. View at Publisher · View at Google Scholar · View at Scopus
  64. E. Schütze and E. Kothe, “Bio-geo interactions in metal-contaminated soils,” in Soil Biology, E. Kothe and A. Varma, Eds., vol. 31, pp. 163–182, Springer, Berlin, Germany, 2012. View at Google Scholar
  65. M. Zhou, X. Jing, P. Xie et al., “Sequential deletion of all the polyketide synthase and nonribosomal peptide synthetase biosynthetic gene clusters and a 900-kb subtelomeric sequence of the linear chromosome of Streptomyces coelicolor,” FEMS Microbiology Letters, vol. 333, no. 2, pp. 169–179, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. L. Diels, P. H. Spaans, S. van Roy et al., “Heavy metals removal by sand filters inoculated with metal sorbing and precipitating bacteria,” Hydrometallurgy, vol. 71, no. 1-2, pp. 235–241, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Ganguli and A. K. Tripathi, “Bioremediation of toxic chromium from electroplating effluent by chromate-reducing Pseudomonas aeruginosa A2Chr in two bioreactors,” Applied Microbiology and Biotechnology, vol. 58, no. 3, pp. 416–420, 2002. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Malik, “Metal bioremediation through growing cells,” Environment International, vol. 30, no. 2, pp. 261–278, 2004. View at Publisher · View at Google Scholar · View at Scopus
  69. W.-L. Smith, “Hexavalent chromium reduction and precipitation by sulphate-reducing bacterial biofilms,” Environmental Geochemistry and Health, vol. 23, no. 3, pp. 297–300, 2001. View at Publisher · View at Google Scholar · View at Scopus
  70. A. S. Y. Ting and C. C. Choong, “Bioaccumulation and biosorption efficacy of Trichoderma isolate SP2F1 in removing copper (Cu(II)) from aqueous solutions,” World Journal of Microbiology and Biotechnology, vol. 25, no. 8, pp. 1431–1437, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. N. Saitou and M. Nei, “The neighbor-joining method: a new method for reconstructing phylogenetic trees,” Molecular Biology and Evolution, vol. 4, no. 4, pp. 406–425, 1987. View at Google Scholar · View at Scopus
  72. K. Tamura, M. Nei, and S. Kumar, “Prospects for inferring very large phylogenies by using the neighbor-joining method,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 30, pp. 11030–11035, 2004. View at Publisher · View at Google Scholar · View at Scopus