Applied Microbiology and Biotechnology

, Volume 87, Issue 4, pp 1271–1280 | Cite as

Metallomics: lessons for metalliferous soil remediation

Mini-Review

Abstract

The term metallomics has been established for the investigation of transcriptome, proteome, and metabolome changes induced by metals. The mechanisms allowing the organisms to cope with metals in the environment, metal resistance factors, will in turn change biogeochemical cycles of metals in soil, coupling the metal pool with the root system of plants. This makes microorganisms key players in introducing metals into food webs, as well as for bioremediation strategies. Research on physiological and metabolic responses of microorganisms on metal stress in soil is thus essential for the selection of optimized consortia applicable in bioremediation strategies such as bioaugmentation or microbially enhanced phytoextraction. The results of metallomics studies will help to develop applications including identification of biomarkers for ecotoxicological studies, bioleaching, in situ soil regeneration, and microbially assisted phytoremediation of contaminated land. This review will therefore focus on the molecular understanding of metal resistance in bacteria and fungi, as can be derived from metallomics studies.

Keywords

Metallomics Proteomics Heavy metal resistance Bioremediation Phytoextraction Biostabilization Bacteria Fungi 

References

  1. Adams P, Lynch JM, De Leij FA (2007) Desorption of zinc by extracellularly produced metabolites of Trichoderma harzianum, Trichoderma reesei and Coriolus versicolor. J Appl Microbiol 103:2240–2247CrossRefGoogle Scholar
  2. Adeyemi AO, Gadd GM (2005) Fungal degradation of calcium-, lead- and silicon-bearing minerals. Biometals 18:269–281CrossRefGoogle Scholar
  3. Albarracín VH, Winik B, Kothe E, Amoroso MJ, Abate CM (2008) Copper bioaccumulation by the actinobacterium Amycolatopsis sp. AB0. J Basic Microbiol 48:323–330CrossRefGoogle Scholar
  4. Alkorta I, Epelde L, Mijangos I, Amezaga I, Garbisu C (2006) Bioluminescent bacterial biosensors for the assessment of metal toxicity and bioavailability in soils. Rev Environ Health 21:139–152Google Scholar
  5. Amoroso MJ, Schubert D, Mitscherlich P, Schumann P, Kothe E (2000) Evidence for high affinity nickel transporter genes in heavy metal resistant Streptomyces spec. J Basic Microbiol 40:295–301CrossRefGoogle Scholar
  6. Audet P, Charest C (2007) Dynamics of arbuscular mycorrhizal symbiosis in heavy metal phytoremediation: meta-analytical and conceptual perspectives. Environ Pollut 147:609–614CrossRefGoogle Scholar
  7. Beauséjour J, Beaulieu C (2004) Characterization of Streptomyces scabies mutants deficient in melanin biosynthesis. Can J Microbiol 50:705–709CrossRefGoogle Scholar
  8. Behl RK, Ruppel S, Kothe E, Narula N (2007) Wheat × Azotobacter × VA Mycorrhiza interactions towards plant nutrition and growth. J Appl Bot 81:95–109Google Scholar
  9. Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. BioMetals 15:325–339CrossRefGoogle Scholar
  10. Bourdineaud JP, Baudrimont M, Gonzalez P, Moreau JL (2006) Challenging the model for induction of metallothionein gene expression. Biochimie 88:1787–1792CrossRefGoogle Scholar
  11. Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207CrossRefGoogle Scholar
  12. Chance MR, Fiser A, Sali A, Pieper U, Eswar N, Xu G, Fajardo JE, Radhakannan T, Marinkovic N (2004) High-throughput computational and experimental techniques in structural genomics. Genome Res 14:2145–2154CrossRefGoogle Scholar
  13. Congeevaram S, Dhanarani S, Park J, Dexilin M, Thamaraiselvi K (2007) Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. J Hazard Mater 146:270–277CrossRefGoogle Scholar
  14. Culotta VC, Joh HD, Lin SJ, Slekar KH, Strain J (1995) A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. J Biol Chem 270:29991–29997CrossRefGoogle Scholar
  15. Cunningham SD, Shann JR, Crowley D, Anderson TA (1997) Phytoremediation of contaminated water and soil. In: Krueger EL, Anderson TA, Coats JP (eds) Phytoremediation of soil and water contaminants. ACS, Washington, pp 2–17CrossRefGoogle Scholar
  16. Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330CrossRefGoogle Scholar
  17. Dickinson RE, Cicerone RJ (1986) Future global warming from atmospheric trace gases. Nature 319:109–115CrossRefGoogle Scholar
  18. Diels L, Van Roy S, Taghavi S, Van Houdt R (2009) From industrial sites to environmental applications with Cupriavidus metallidurans. Antonie Van Leeuwenhoek 96:247–258CrossRefGoogle Scholar
  19. Diesel E, Schreiber M, van der Meer JR (2009) Development of bacteria-based bioassays for arsenic detection in natural waters. Anal Bioanal Chem 394:687–693CrossRefGoogle Scholar
  20. Dimkpa C, Svatos A, Merten D, Büchel G, Kothe E (2008a) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54:163–172CrossRefGoogle Scholar
  21. Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008b) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19–25CrossRefGoogle Scholar
  22. Dimkpa CO, Merten D, Svatos A, Büchel G, Kothe E (2009) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696CrossRefGoogle Scholar
  23. Dudka S, Adriano DC (1997) Environmental impacts of metal ore mining and processing: a review. J Environ Qual 26:590–602CrossRefGoogle Scholar
  24. Fomina M, Gadd GM (2003) Metal sorption by biomass of melanin-producing fungi grown in clay-containing medium. J Chem Technol Biotechnol 78:23–34CrossRefGoogle Scholar
  25. Fomina M, Hillier S, Charnock JM, Melville K, Alexander IJ, Gadd GM (2005) Role of oxalic acid overexcretion in transformations of toxic metal minerals by Beauveria caledonica. Appl Environ Microbiol 71:371–381CrossRefGoogle Scholar
  26. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36CrossRefGoogle Scholar
  27. Furrer G, Phillips BL, Ulrich KU, Pöthig R, Casey WH (2002) The origin of aluminum flocs in polluted streams. Science 297:2245–2247CrossRefGoogle Scholar
  28. Gadd GM (1999) Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Adv Microb Physiol 41:47–92CrossRefGoogle Scholar
  29. Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49CrossRefGoogle Scholar
  30. Gadd GM (2009) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643CrossRefGoogle Scholar
  31. Garcia JS, Magalhães CS, Arruda MA (2006) Trends in metal-binding and metalloprotein analysis. Talanta 69:1–15CrossRefGoogle Scholar
  32. Geslin C, Llanos J, Prieur D, Jeanthon C (2001) The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res Microbiol 152:901–905CrossRefGoogle Scholar
  33. Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122CrossRefGoogle Scholar
  34. Goldsbrough P, Cobbett C (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182CrossRefGoogle Scholar
  35. González-Fernández M, García-Barrera T, Arias-Borrego A, Jurado J, Pueyo C, López-Barea J, Gómez-Ariza JL (2009) Metallomics integrated with proteomics in deciphering metal-related environmental issues. Biochimie 91:1311–1317CrossRefGoogle Scholar
  36. Grande JA, Beltrán R, Sáinz A, Santos JC, de la Torre ML, Borrego J (2005) Acid mine drainage and acid rock drainage processes in the environment of Herrerías Mine (Iberian Pyrite Belt, Huelva-Spain) and impact on the Andevalo Dam. Environ Geol 47:185–196CrossRefGoogle Scholar
  37. Gutiérrez JC, Amaro F, Martín-González A (2009) From heavy metal-binders to biosensors: ciliate metallothioneins discussed. Bioessays 31:805–816CrossRefGoogle Scholar
  38. Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467CrossRefGoogle Scholar
  39. Haferburg G, Merten D, Büchel G, Kothe E (2007) Biosorption of metal and salt tolerant microbial isolates from a former uranium mining area. Their impact on changes in rare earth element patterns in acid mine drainage. J Basic Microbiol 47:474–484CrossRefGoogle Scholar
  40. Haferburg G, Kloess G, Schmitz W, Kothe E (2008) “Ni-struvite”—a new biomineral formed by a nickel resistant Streptomyces acidiscabies. Chemosphere 72:517–523CrossRefGoogle Scholar
  41. Haferburg G, Groth I, Möllmann U, Kothe E, Sattler I (2009) Arousing sleeping genes: shifts in secondary metabolism of metal tolerant actinobacteria under conditions of heavy metal stress. Biometals 22:225–234CrossRefGoogle Scholar
  42. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146CrossRefGoogle Scholar
  43. Hirata K, Tsuji N, Miyamoto K (2005) Biosynthetic regulation of phytochelatins, heavy metal-binding peptides. J Biosci Bioeng 100:593–599CrossRefGoogle Scholar
  44. Iordache V, Gherghel F, Kothe E (2009) Assessing the effect of disturbances on ectomycorrhiza diversity. Int J Environ Res Public Health 6:414–432CrossRefGoogle Scholar
  45. Jiang K, Sun TH, Sun LN, Li HB (2006) Adsorption characteristics of copper, lead, zinc and cadmium ions by tourmaline. J Environ Sci 18:1221–1225CrossRefGoogle Scholar
  46. Keller C, Ludwig C, Davoli F, Wochele J (2005) Thermal treatment of metal-enriched biomass produced from heavy metal phytoextraction. Environ Sci Technol 39:3359–3367CrossRefGoogle Scholar
  47. Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364CrossRefGoogle Scholar
  48. Khan AG (2006) Mycorrhizoremediation—an enhanced form of phytoremediation. J Zhejiang Univ Sci B 7:503–514CrossRefGoogle Scholar
  49. Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522CrossRefGoogle Scholar
  50. Liang CC, Li T, Xiao YP, Liu MJ, Zhang HB, Zhao ZW (2009a) Effects of inoculation with arbuscular mycorrhizal fungi on maize grown in multi-metal contaminated soils. Int J Phytorem 11:692–703CrossRefGoogle Scholar
  51. Liang HM, Lin TH, Chiou JM, Yeh KC (2009b) Model evaluation of the phytoextraction potential of heavy metal hyperaccumulators and non-hyperaccumulators. Environ Pollut 157:1945–1952CrossRefGoogle Scholar
  52. Lobinski R, Moulin C, Ortega R (2006) Imaging and speciation of trace elements in biological environment. Biochimie 88:1591–1604CrossRefGoogle Scholar
  53. López-Barea J, Gómez-Ariza JL (2006) Environmental proteomics and metallomics. Proteomics Suppl 1:51–62CrossRefGoogle Scholar
  54. Magyarosy A, Laidlaw RD, Kilaas R, Echer C, Clark DS, Keasling JD (2002) Nickel accumulation and nickel oxalate precipitation by Aspergillus niger. Appl Microbiol Biotechnol 59:382–388CrossRefGoogle Scholar
  55. Mellano MA, Cooksey DA (1988) Induction of the copper resistance operon from Pseudomonas syringae. J Bacteriol 170:4399–4401Google Scholar
  56. Mounicou S, Szpunar J, Lobinski R (2009) Metallomics: the concept and methodology. Chem Soc Rev 38:1119–1138CrossRefGoogle Scholar
  57. Muñoz AH, Kubachka K, Wrobel K, Corona FG, Yathavakilla SK, Caruso JA, Wrobel K (2005) Metallomics approach to trace element analysis in Ustilago maydis using cellular fractionation, atomic absorption spectrometry, and size exclusion chromatography with ICP-MS detection. J Agric Food Chem 53:5138–5143CrossRefGoogle Scholar
  58. Narula N, Kothe E, Behl RK (2009) Role of root exudates in plant–microbe interactions. J Appl Bot Food Qual 82:122–130Google Scholar
  59. Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750CrossRefGoogle Scholar
  60. Nriagu JA (1996) A history of global metal pollution. Science 272:223–224CrossRefGoogle Scholar
  61. Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649CrossRefGoogle Scholar
  62. Pan R, Cao L, Zhang R (2009) Combined effects of Cu, Cd, Pb, and Zn on the growth and uptake of consortium of Cu-resistant Penicillium sp. A1 and Cd-resistant Fusarium sp. A19. J Hazard Mater 171:761–766CrossRefGoogle Scholar
  63. Parvez S, Venkataraman C, Mukherji S (2006) A review on advantages of implementing luminescence inhibition test (Vibrio fischeri) for acute toxicity prediction of chemicals. Environ Int 32:265–268CrossRefGoogle Scholar
  64. Peters RW (1999) Chelant extraction of heavy metals from contaminated soils. J Hazard Mater 66:151–210CrossRefGoogle Scholar
  65. Poynton HC, Varshavsky JR, Chang B, Cavigiolio G, Chan S, Holman PS, Loguinov AV, Bauer DJ, Komachi K, Theil EC, Perkins EJ, Hughes O, Vulpe CD (2007) Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ Sci Technol 41:1044–1050CrossRefGoogle Scholar
  66. Prasad MN, Freitas H, Fraenzle S, Wuenschmann S, Markert B (2010) Knowledge explosion in phytotechnologies for environmental solutions. Environ Pollut 158:18–23CrossRefGoogle Scholar
  67. Robinson NJ, Whitehall SK, Cavet JS (2001) Microbial metallothioneins. Adv Microb Physiol 44:183–213CrossRefGoogle Scholar
  68. Sayer JA, Kierans M, Gadd GM (1997) Solubilisation of some naturally occurring metal-bearing minerals, limescale and lead phosphate by Aspergillus niger. FEMS Microbiol Lett 154:29–35CrossRefGoogle Scholar
  69. Schachtschabel P, Blume HP, Brümmer G, Hartge KH, Schwertmann U (1998) Lehrbuch der Bodenkunde. Enke, StuttgartGoogle Scholar
  70. Schmidt A, Schmidt A, Haferburg G, Kothe E (2007) Superoxide dismutases of heavy metal resistant streptomycetes. J Basic Microbiol 47:56–62CrossRefGoogle Scholar
  71. Schmidt A, Gube M, Schmidt A, Kothe E (2009) In silico analysis of nickel containing superoxide dismutase evolution and regulation. J Basic Microbiol 49:109–118CrossRefGoogle Scholar
  72. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365CrossRefGoogle Scholar
  73. Shen H, Christie P, Li X (2006) Uptake of zinc, cadmium and phosphorus by arbuscular mycorrhizal maize (Zea mays L.) from a low available phosphorus calcareous soil spiked with zinc and cadmium. Environ Geochem Health 28:111–119CrossRefGoogle Scholar
  74. Silver S (1996) Bacterial resistances to toxic metal ions—a review. Gene 179:9–19CrossRefGoogle Scholar
  75. Silver S, Phung LT (1996) Bacterial heavy metals resistance: new surprises. Annu Rev Microbiol 50:753–789CrossRefGoogle Scholar
  76. Siñeriz ML, Kothe E, Abate CM (2009) Cadmium biosorption by Streptomyces sp. F4 isolated from former uranium mine. J Basic Microbiol 49(Suppl1):S55–S62Google Scholar
  77. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San DiegoGoogle Scholar
  78. Sobolev D, Begonia MF (2008) Effects of heavy metal contamination upon soil microbes: lead induced changes in general and denitrifying microbial communities as evidenced by molecular markers. Int J Environ Res Public Health 5:450–456CrossRefGoogle Scholar
  79. Sprocati AR, Alisi C, Segre L, Tasso F, Galletti M, Cremisini C (2006) Investigating heavy metal resistance, bioaccumulation and metabolic profile of a metallophile microbial consortium native to an abandoned mine. Sci Total Environ 366:649–658CrossRefGoogle Scholar
  80. Szpunar J (2004) Metallomics: a new frontier in analytical chemistry. Anal Bioanal Chem 378:54–56CrossRefGoogle Scholar
  81. Szpunar J (2005) Advances in analytical methodology for bioinorganic speciation analysis: metallomics, metalloproteomics and heteroatom-tagged proteomics and metabolomics. Analyst 30:442–465CrossRefGoogle Scholar
  82. Tchize Ndejouong BLS, Sattler I, Dahse HM, Kothe E, Hertweck C (2009) Isoflavones with unusually modified b-rings and their evaluation as antiproliferative agents. Bioorg Med Chem Lett 19:6473–6476CrossRefGoogle Scholar
  83. Ulrich B, Benzler JH (1955) Der organisch gebundene Phosphor im Boden. Z Pflanzenernähr Düng Bodenk 70:220CrossRefGoogle Scholar
  84. Vielle-Calzada JP, Martínez de la Vega O, Hernández-Guzmán G, Ibarra-Laclette E, Alvarez-Mejía C, Vega-Arreguín JC, Jiménez-Moraila B, Fernández-Cortés A, Corona-Armenta G, Herrera-Estrella L, Herrera-Estrella A (2009) The Palomero genome suggests metal effects on domestication. Science 326:1078CrossRefGoogle Scholar
  85. Vijayaraghavan K, Yun YS (2008) Bacterial biosorbents and biosorption. Biotechnol Adv 26:266–291CrossRefGoogle Scholar
  86. Virta M, Tauriainen S, Karp M (1998) Bioluminescence-based metal detectors. Methods Mol Biol 102:219–229Google Scholar
  87. Vivas A, Moreno B, del Val C, Macci C, Masciandaro G, Benitez E (2008) Metabolic and bacterial diversity in soils historically contaminated by heavy metals and hydrocarbons. J Environ Monit 10:1287–1296CrossRefGoogle Scholar
  88. Wang J, Chen C (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol Adv 24:427–451CrossRefGoogle Scholar
  89. Wang FY, Lin XG, Yin R (2007a) Role of microbial inoculation and chitosan in phytoextraction of Cu, Zn, Pb and Cd by Elsholtzia splendens—a field case. Environ Pollut 147:248–255CrossRefGoogle Scholar
  90. Wang FY, Lin XG, Yin R (2007b) Effect of arbuscular mycorrhizal fungal inoculation on heavy metal accumulation of maize grown in a naturally contaminated soil. Int J Phytorem 9:345–353CrossRefGoogle Scholar
  91. Wengel M, Kothe E, Schmidt CM, Heide K, Gleixner G (2006) Degradation of organic matter from black shales and charcoal by the wood-rotting fungus Schizophyllum commune and release of DOC and heavy metals in the aqueous phase. Sci Total Environ 367:383–393CrossRefGoogle Scholar
  92. White C, Sayer JA, Gadd GM (1997) Microbial solubilization and immobilization of toxic metals: key biogeochemical processes for treatment of contamination. FEMS Microbiol Rev 20:503–516CrossRefGoogle Scholar
  93. Zeien H, Brümmer GW (1989) Chemische Extraktionen zur Bestimmung von Schwermetallbindungsformen in Böden. Mitt Dtsch Bodenkd Ges 59:505–510Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Institute of MicrobiologyFriedrich Schiller UniversityJenaGermany

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