Toxic Metal/Metalloid Tolerance in Fungi—A Biotechnology-Oriented Approach

Chapter

Abstract

This review aims at the biotechnological evaluation of the wealth of data accumulated in the last decade on the molecular background of the toxic metal/metalloid tolerance of fungi. Yeast-based models are highly applicable when metal/metalloid transport and compartmentalization processes are mapped in other fungal species or higher eukaryotes but this approach has limitations, which necessitates further fungal models evolutionarily closer to heavy metal exposed fungal taxons. In terms of biotechnology, the most promising targets in the genetic engineering of metal/metalloid tolerant fungi include (i) increased secretion of extracellular metal chelators , (ii) elimination of metal transporters facilitating the uptake of toxic metals/metalloids, (iii) overexpression of transporters pumping metals and/or their complexes out of the cells or into cellular organelles, (iv) overproduction of intracellular metal chelators , (v) overproduction of elements of the antioxidative defense system, (vi) genetic modification of the regulatory network of metal/metalloid stress defense, and (vii) interfering with the metal/metalloid-dependent initialization of apoptotic cell death. Owing to the wide-spread application of robust ‘-omics’ technologies, the biotechnologically exploitable data including potential future targets for genetic manipulation are accumulating fast. In contrast, today’s genetic modifications often result in unforeseeable or even paradox phenotypes in this field, which clearly indicates that a deeper understanding of the underlying molecular mechanisms of fungal toxic metal/metalloid tolerance is needed to improve the biotechnological performance of the genetically modified strains.

Keywords

Arbuscular Mycorrhizal Fungus Heavy Metal Tolerance Pullulan Production Chronological Life Span Pichia Guilliermondii 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgement

The author is indebted to Dr. M. J. Tamás, University of Gothenburg, for reading critically the manuscript.

References

  1. Adamec J, Rusnak F, Owen WG, Naylor S, Benson LM, Gacy AM, Isaya G (2000) Iron-dependent self-assembly of recombinant yeast frataxin: implications for Friedreich ataxia. Am J Hum Genet 67:549–562PubMedCrossRefGoogle Scholar
  2. Adamis PD, Mannarino SC, Riger CJ, Duarte G, Cruz A, Pereira MD, Eleutherio EC (2009) Lap4, a vacuolar aminopeptidase I, is involved in cadmium-glutathione metabolism. Biometals 22:243–249PubMedCrossRefGoogle Scholar
  3. Adle DJ, Sinani D, Kim H, Lee J (2007) A cadmium-transporting P1B-type ATPase in yeast Saccharomyces cerevisiae. J Biol Chem 282:947–955PubMedCrossRefGoogle Scholar
  4. Adriaensen K, Vrålstad T, Noben JP, Vangronsveld J, Colpaert JV (2005) Copper-adapted Suillus luteus, a symbiotic solution for pines colonizing Cu mine spoils. Appl Environ Microbiol 71:7279–7284PubMedCrossRefGoogle Scholar
  5. Adriaensen K, Vangronsveld J, Colpaert JV (2006) Zinc-tolerant Suillus bovinus improves growth of Zn-exposed Pinus sylvestris seedlings. Mycorrhiza 16:553–558PubMedCrossRefGoogle Scholar
  6. Agrawal A, Kumar V, Pandey BD (2006) Remediation options for the treatment of electroplating and leather tanning effluent containing chromium—a review. Mineral Proc Extr Metall Rev 27:99–130CrossRefGoogle Scholar
  7. Aloui A, Recorbet G, Gollotte A, Robert F, Valot B, Gianinazzi-Pearson V, Aschi-Smiti S, Dumas-Gaudot E (2009) On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: a root proteomic study. Proteomics 9:420–433PubMedCrossRefGoogle Scholar
  8. Avery SV (2001) Metal toxicity in yeasts and the role of oxidative stress. Adv Appl Microbiol 49:111–142PubMedCrossRefGoogle Scholar
  9. Azevedo D, Nascimento L, Labarre J, Toledano MB, Rodrigues-Pousada C (2007) The S. cerevisiae Yap1 and Yap2 transcription factors share a common cadmium-sensing domain. FEBS Lett 581:187–195PubMedCrossRefGoogle Scholar
  10. Azevedo MM, Almeida B, Ludovico P, Cássio F (2009) Metal stress induces programmed cell death in aquatic fungi. Aquat Toxicol 92:264–270PubMedCrossRefGoogle Scholar
  11. Bae W, Chen X (2004) Proteomic study for the cellular responses to Cd2+ in Schizosaccharomyces pombe through amino acid-coded mass tagging and liquid chromatography tandem mass spectrometry. Mol Cell Proteomics 3:596–607PubMedCrossRefGoogle Scholar
  12. Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzyme Microb Technol 32:78–91CrossRefGoogle Scholar
  13. Bellion M, Courbot M, Jacob C, Guinet F, Blaudez D, Chalot M (2007) Metal induction of a Paxillus involutus metallothionein and its heterologous expression in Hebeloma cylindrosporum. New Phytol 174:151–158PubMedCrossRefGoogle Scholar
  14. Bhainsa KC, D’Souza SF (2006) Extracellular biosynthesis of silver nanoparticles using the fungus Aspergillus fumigatus. Colloids Surf B Biointerfaces 47:160–164PubMedCrossRefGoogle Scholar
  15. Binupriya AR, Sathishkumar M, Vijayaraghavan K, Yun SI (2010) Bioreduction of trivalent aurum to nano-crystalline gold particles by active and inactive cells and cell-free extract of Aspergillus oryzae var. viridis. J Hazard Mater 177:539–545PubMedCrossRefGoogle Scholar
  16. Blaiseau PL, Lesuisse E, Camadro JM (2001) Aft2p, a novel iron-regulated transcription activator that modulates, with Aft1p, intracellular iron use and resistance to oxidative stress in yeast. J Biol Chem 276:34221–34226.PubMedCrossRefGoogle Scholar
  17. Boretsky YR, Protchenko OV, Prokopiv TM, Mukalov IO, Fedorovych DV, Sibirny AA (2007) Mutations and environmental factors affecting regulation of riboflavin synthesis and iron assimilation also cause oxidative stress in the yeast Pichia guilliermondii. J Basic Microbiol 47:371–377PubMedCrossRefGoogle Scholar
  18. Borghouts C, Werner A, Elthon T, Osiewacz HD (2001) Copper-modulated gene expression and senescence in the filamentous fungus Podospora anserina. Mol Cell Biol 21:390–399PubMedCrossRefGoogle Scholar
  19. Borrelly GP, Harrison MD, Robinson AK, Cox SG, Robinson NJ, Whitehall SK (2002) Surplus zinc is handled by Zym1 metallothionein and Zhf endoplasmic reticulum transporter in Schizosaccharomyces pombe. J Biol Chem 277:30394–30400PubMedCrossRefGoogle Scholar
  20. Bothe H, Regvar M, Turnau K (2010) Arbuscular mycorrhiza, heavy metal, and salt tolerance. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Berlin, pp 87–111Google Scholar
  21. Breierová E, Gregor T, Juršíková P, Stratilová E, Fišera M (2004) The role of pullulan and pectin in the uptake of Cd2+ and Ni2+ ions by Aureobasidium pullulans. Ann Microbiol 54:247–255Google Scholar
  22. Brown NM, Torres AS, Doan PE, O’Halloran TV (2004) Oxygen and the copper chaperone CCS regulate posttranslational activation of Cu,Zn superoxide dismutase. Proc Natl Acad Sci U S A 101:5518–5523PubMedCrossRefGoogle Scholar
  23. Bučková M, Godočíková J, Šimonovičová A, Polek B (2005) Production of catalases by Aspergillus niger isolates as a response to pollutant stress by heavy metals. Curr Microbiol 50:175–179PubMedCrossRefGoogle Scholar
  24. Bulteau AL, O’Neill HA, Kennedy MC, Ikeda-Saito M, Isaya G, Szweda LI (2004) Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 305:242–245Google Scholar
  25. Bun-ya M, Harashima S, Oshima Y (1992) Putative GTP-binding protein, Gtr1, associated with the function of the Pho84 inorganic phosphate transporter in Saccharomyces cerevisiae. Mol Cell Biol 12:2958–2966PubMedGoogle Scholar
  26. Bun-ya M, Shikata K, Nakade S, Yompakdee C, Harashima S, Oshima Y (1996) Two new genes, PHO86 and PHO87, involved in inorganic phosphate uptake in Saccharomyces cerevisiae. Curr Genet 29:344–351PubMedGoogle Scholar
  27. Campanella A, Isaya G, O'Neill HA, Santambrogio P, Cozzi A, Arosio P, Levi S (2004) The expression of human mitochondrial ferritin rescues respiratory function in frataxin-deficient yeast. Hum Mol Genet 13:2279–2288Google Scholar
  28. Cánovas D, de Lorenzo V (2007) Osmotic stress limits arsenic hypertolerance in Aspergillus sp. P37. FEMS Microbiol Ecol 61:258–263CrossRefGoogle Scholar
  29. Cánovas D, Mukhopadhyay R, Rosen BP, de Lorenzo V (2003) Arsenate transport and reduction in the hyper-tolerant fungus Aspergillus sp. P37. Environ Microbiol 5:1087–1093PubMedCrossRefGoogle Scholar
  30. Cánovas D, Vooijs R, Schat H, de Lorenzo V (2004) The role of thiol species in the hypertolerance of Aspergillus sp. P37 to arsenic. J Biol Chem 279:51234–51240PubMedCrossRefGoogle Scholar
  31. Čertik M, Breierová E, Juršíková P (2005) Effect of cadmium on lipid composition of Aureobasidium pullulans grown with added extracellular polysaccharides. Int Biodeter Biodegr 55:195–202CrossRefGoogle Scholar
  32. Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443PubMedCrossRefGoogle Scholar
  33. Chatterjee N, Luo Z (2010) Cr-(III)-organic compounds treatment causes genotoxicity and changes in DNA and protein level in Saccharomyces cerevisiae. Ecotoxicology 19:593–603PubMedCrossRefGoogle Scholar
  34. Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bähler J (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 1:214–229CrossRefGoogle Scholar
  35. Chen YL, Tuan HY, Tien CW, Lo WH, Liang HC, Hu YC (2009) Augmented biosynthesis of cadmium sulfide nanoparticles by genetically engineered Escherichia coli. Biotechnol Prog 25:1260–1266PubMedCrossRefGoogle Scholar
  36. Cherest H, Davidian JC, Thomas D, Benes V, Ansorge W, Surdin-Kerjan Y (1997) Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics 145:627–635PubMedGoogle Scholar
  37. Chuang HW, Wang IW, Lin SY, Chang YL (2009) Transcriptome analysis of cadmium response in Ganoderma lucidum. FEMS Microbiol Lett 293:205–213PubMedCrossRefGoogle Scholar
  38. Clausen CA, Green F (2003) Oxalic acid overproduction by copper-tolerant brown rot basidiomycetes on southern yellow pine treated with copper-based preservatives. Int Biodeter Biodegr 51:139–144CrossRefGoogle Scholar
  39. Clemens S, Kim EJ, Neumann D, Schroeder JI (1999) Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J 18:3325–3333PubMedCrossRefGoogle Scholar
  40. Conklin DS, McMaster JA, Culbertson MR, Kung C (1992) COT1, a gene involved in cobalt accumulation in Saccharomyces cerevisiae. Mol Cell Biol 12:3678–3688PubMedGoogle Scholar
  41. Conklin DS, Culbertson MR, Kung C (1994) Interactions between gene products involved in divalent cation transport in Saccharomyces cerevisiae. Mol Gen Genet 244:303–311PubMedCrossRefGoogle Scholar
  42. Coreño-Alonso A, Acevedo-Aguilar FJ, Reyna-López GE, Tomasini A, Fernández FJ, Wrobel K, Gutiérrez-Corona JF (2009) Cr(VI) reduction by an Aspergillus tubingensis strain: role of carboxylic acids and implications for natural attenuation and biotreatment of Cr(VI) contamination. Chemosphere 76:43–47PubMedCrossRefGoogle Scholar
  43. Cornejo P, Meier S, Borie G, Rillig MC, Borie F (2008) Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Sci Total Environ 406:154–160PubMedCrossRefGoogle Scholar
  44. Corson LB, Folmer J, Strain JJ, Culotta VC, Cleveland DW (1999) Oxidative stress and iron are implicated in fragmenting vacuoles of Saccharomyces cerevisiae lacking Cu,Zn-superoxide dismutase. J Biol Chem 274:27590–27596PubMedCrossRefGoogle Scholar
  45. Courbot M, Diez L, Ruotolo R, Chalot M, Leroy P (2004) Cadmium responsive thiols in the ectomycorrhizal fungus Paxillus involutus. Appl Environ Microbiol 70:7413–7417PubMedCrossRefGoogle Scholar
  46. 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 270:29991–29997PubMedCrossRefGoogle Scholar
  47. Dainty SJ, Kennedy CA, Watt S, Bähler J, Whitehall SK (2008) Response of Schizosaccharomyces pombe to zinc deficiency. Eukaryot Cell 7:454–464PubMedCrossRefGoogle Scholar
  48. Dameron CT, Reese RN, Mehra RK, Kortan AR, Carroll PJ, Steigerwald ML, Brus LE, Winge DR (1989) Biosynthesis of cadmium-sulfide quantum semiconductor crystallites. Nature 338:696–597CrossRefGoogle Scholar
  49. De Freitas JM, Liba A, Meneghini R, Valentine JS, Gralla EB (2000) Yeast lacking Cu-Zn superoxide dismutase show altered iron homeostasis. Role of oxidative stress in iron metabolism. J Biol Chem 275:1645–11649CrossRefGoogle Scholar
  50. De Freitas J, Wintz H, Kim JH, Poynton H, Fox T, Vulpe C (2003) Yeast, a model organism for iron and copper metabolism studies. Biometals 16:185–197PubMedCrossRefGoogle Scholar
  51. Desmyter L, Dewaele S, Reekmans R, Nystrom T, Contreras R, Chen C (2008) Expression of the human ferritin light chain in a frataxin mutant yeast affects ageing and cell death. Exp Gerontol 39:707–715CrossRefGoogle Scholar
  52. Deepa KK, Sathishkumar M, Binupriya AR, Murugesan GS, Swaminathan K, Yun SE (2006) Sorption of Cr(VI) from dilute solutions and wastewater by live and pretreated biomass of Aspergillus flavus. Chemosphere 62:833–840PubMedCrossRefGoogle Scholar
  53. Dilda PJ, Perrone GG, Philp A, Lock RB, Dawes IW, Hogg PJ (2008) Insight into the selectivity of arsenic trioxide for acute promyelocytic leukemia cells by characterizing Saccharomyces cerevisiae deletion strains that are sensitive or resistant to the metalloid. Int J Biochem Cell Biol 40:1016–1029PubMedCrossRefGoogle Scholar
  54. Ecker DJ, Butt TR, Sternberg EJ, Neeper MP, Debouck C, Gorman JA, Crooke ST (1986) Yeast metallothionein function in metal ion detoxification. J Biol Chem 261:16895–16900PubMedGoogle Scholar
  55. Eisenberg T, Büttner S, Kroemer G, Madeo F (2007) The mitochondrial pathway in yeast apoptosis. Apoptosis 12:1011–1023PubMedCrossRefGoogle Scholar
  56. Eisendle M, Oberegger H, Zadra I, Haas H (2003) The siderophore system is essential for viability of Aspergillus nidulans: functional analysis of two genes encoding L-ornithine N5-monooxygenase (sidA) and a non-ribosomal peptide synthetase (sidC). Mol Microbiol 49:359–375PubMedCrossRefGoogle Scholar
  57. Eisendle M, Schrettl M, Kragl C, Müller D, Illmer P, Haas H (2006) The intracellular siderophore ferricrocin is involved in iron storage, oxidative-stress resistance, germination, and sexual development in Aspergillus nidulans. Eukaryot Cell 5:1596–1603PubMedCrossRefGoogle Scholar
  58. Enjalbert B, Smith DA, Cornell MJ, Alam I, Nicholls S, Brown AJ, Quinn J (2006) Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol Biol Cell 17:1018–1032PubMedCrossRefGoogle Scholar
  59. Enyedy EA, Pócsi I, Farkas E (2004) Complexation of desferricoprogen with trivalent Fe, Al, Ga, In and divalent Fe, Ni, Cu, Zn metal ions: effects of the linking chain structure on the metal binding ability of hydroxamate based siderophores. J Inorg Biochem 98:1957–1966PubMedCrossRefGoogle Scholar
  60. Farkas E, Bátka D, Kremper G, Pócsi I (2008) Structure-based differences between the metal ion selectivity of two siderophores desferrioxamine B (DFB) and desferricoprogen (DFC): why DFC is much better Pb(II) sequestering agent than DFB? J Inorg Biochem 102:1654–1659PubMedCrossRefGoogle Scholar
  61. Fauchon M, Lagniel G, Aude JC, Lombardia L, Soularue P, Petat C, Marguerie G, Sentenac A, Werner M, Labarre J (2002) Sulfur sparing in the yeast proteome in response to sulfur demand. Mol Cell 9:713–723PubMedCrossRefGoogle Scholar
  62. Fei L, Wang Y, Chen S (2009) Improved GSH production by gene expression in Pichia pastoris. Bioproc Biosyst Eng 32:729–735CrossRefGoogle Scholar
  63. Ferrol N, González-Guerrero M, Valderas A, Benabdellah K, Azcón-Aguilar C (2009) Survival strategies of arbuscular mycorrhizal fungi in Cu-polluted environments. Phytochem Rev 8:551–559CrossRefGoogle Scholar
  64. Foury F, Talibi D (2001) Mitochondrial control of iron homeostasis. A genome wide analysis of gene expression in a yeast frataxin-deficient strain. J Biol Chem 276:7762–7768PubMedCrossRefGoogle Scholar
  65. Fraser JA, Davis MA, Hynes MJ (2002) A gene from Aspergillus nidulans with similarity to URE2 of Saccharomyces cerevisiae encodes a glutathione S-transferase which contributes to heavy metal and xenobiotic resistance. Appl Environ Microbiol 68:2802–2808PubMedCrossRefGoogle Scholar
  66. Fujii K, Fukunaga S (2008) Isolation of highly copper-tolerant fungi from the smelter of the Naganobori copper mine, an historic mine in Japan. J Appl Microbiol 105:1851–1857PubMedCrossRefGoogle Scholar
  67. Fukuda T, Ishino Y, Ogawa A, Tsutsumi K, Morita H (2008) Cr(VI) reduction from contaminated soils by Aspergillus sp. N2 and Penicillium sp. N3 isolated from chromium deposits. J Gen Appl Microbiol 54:295–303Google Scholar
  68. Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279PubMedCrossRefGoogle Scholar
  69. Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643PubMedCrossRefGoogle Scholar
  70. Gakh O, Park S, Liu G, Macomber L, Imlay JA, Ferreira GC, Isaya G (2006) Mitochondrial iron detoxification is a primary function of frataxin that limits oxidative damage and preserves cell longevity. Hum Mol Genet 15:467–479PubMedCrossRefGoogle Scholar
  71. Gakh O, Smith DY 4th, Isaya G (2008) Assembly of the iron-binding protein frataxin in Saccharomyces cerevisiae responds to dynamic changes in mitochondrial iron influx and stress level. J Biol Chem 283:31500–31510PubMedCrossRefGoogle Scholar
  72. Gardarin A, Chédin S, Lagniel G, Aude JC, Godat E, Catty P, Labarre J (2010) Endoplasmic reticulum is a major target of cadmium toxicity in yeast. Mol Microbiol 76:1034–1048PubMedCrossRefGoogle Scholar
  73. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257PubMedGoogle Scholar
  74. Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534Google Scholar
  75. Gazdag Z, Pócsi I, Belágyi J, Emri T, Blaskó A, Takács K, Pesti M (2003) Chromate tolerance caused by reduced hydroxyl radical production and decreased glutathione reductase activity in Schizosaccharomyces pombe. J Basic Microbiol 43:96–103PubMedCrossRefGoogle Scholar
  76. Georg RC, Gomes SL (2007) Transcriptome analysis in response to heat shock and cadmium in the aquatic fungus Blastocladiella emersonii. Eukaryot Cell 6:1053–1062PubMedCrossRefGoogle Scholar
  77. Gitan RS, Luo H, Rodgers J, Broderius M, Eide D (1998) Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. J Biol Chem 273:28617–28624PubMedCrossRefGoogle Scholar
  78. Gitan RS, Shababi M, Kramer M, Eide DJ (2003) A cytosolic domain of the yeast Zrt1 zinc transporter is required for its post-translational inactivation in response to zinc and cadmium. J Biol Chem 278:39558–39564PubMedCrossRefGoogle Scholar
  79. Gomes DS, Fragoso LC, Riger CJ, Panek AD, Eleutherio EC (2002) Regulation of cadmium uptake by Saccharomyces cerevisiae. Biochim Biophys Acta 1573:21–25PubMedCrossRefGoogle Scholar
  80. González-Chávez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323PubMedCrossRefGoogle Scholar
  81. González-Guerrero M, Azcón-Aguilar C, Mooney M, Valderas A, MacDiarmid CW, Eide DJ, Ferrol N (2005) Characterization of a Glomus intraradices gene encoding a putative Zn transporter of the cation diffusion facilitator family. Fungal Genet Biol 42:130–140PubMedCrossRefGoogle Scholar
  82. González-Guerrero M, Cano C, Azcón-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335PubMedCrossRefGoogle Scholar
  83. González-Guerrero M, Melville LH, Ferrol N, Lott JN, Azcón-Aguilar C, Peterson RL (2008) Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices. Can J Microbiol 54:103–110PubMedCrossRefGoogle Scholar
  84. González-Guerrero M, Benabdellah K, Ferrol N, Azcón-Aguilar C (2009) Mechanisms underlying heavy metal tolerance in arbuscular mycorrhizas. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas—Functional Processes and Ecological Impacts. Springer, Berlin, pp 107–122CrossRefGoogle Scholar
  85. González-Guerrero M, Benabdellah K, Valderas A, Azcón-Aguilar C, Ferrol N (2010a) GintABC1 encodes a putative ABC transporter of the MRP subfamily induced by Cu, Cd, and oxidative stress in Glomus intraradices. Mycorrhiza 20:137–146CrossRefGoogle Scholar
  86. González-Guerrero M, Oger E, Benabdellah K, Azcón-Aguilar C, Lanfranco L, Ferrol N (2010b) Characterization of a CuZn superoxide dismutase gene in the arbuscular mycorrhizal fungus Glomus intraradices. Curr Genet 56:265–274CrossRefGoogle Scholar
  87. Gorfer M, Persak H, Berger H, Brynda S, Bandian D, Strauss J (2009) Identification of heavy metal regulated genes from the root associated ascomycete Cadophora finlandica using a genomic microarray. Mycol Res 113:1377–1388PubMedCrossRefGoogle Scholar
  88. Gross C, Kelleher M, Iyer VR, Brown PO, Winge DR (2000) Identification of the copper regulon in Saccharomyces cerevisiae by DNA microarrays. J Biol Chem 275:32310–32316PubMedCrossRefGoogle Scholar
  89. Guo J, Dai X, Xu W, Ma M (2008) Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere 72:1020–1026PubMedCrossRefGoogle Scholar
  90. Harris N, Bachler M, Costa V, Mollapour M, Moradas-Ferreira P, Piper PW (2005) Overexpressed Sod1p acts either to reduce or to increase the lifespans and stress resistance of yeast, depending on whether it is Cu2+-deficient or an active Cu,Zn-superoxide dismutase. Aging Cell 4:41–52PubMedCrossRefGoogle Scholar
  91. Haugen AC, Kelley R, Collins JB, Tucker CJ, Deng C, Afshari CA, Brown JM, Ideker T, Van Houten B (2004) Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biol 5:R95CrossRefGoogle Scholar
  92. Hegedűs N, Emri T, Szilágyi J, Karányi Zs, Nagy I, Penninckx MJ, Pócsi I (2007) Effect of heavy metals on the GSH status in different ectomycorrhizal Paxillus involutus strains. World J Microbiol Biotechnol 23:1339–1343CrossRefGoogle Scholar
  93. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146PubMedCrossRefGoogle Scholar
  94. Hirata D, Yano K, Miyakawa T (1994) Stress-induced transcriptional activation mediated by YAP1 and YAP2 genes that encode the Jun family of transcriptional activators in Saccharomyces cerevisiae. Mol Gen Genet 242:250–256PubMedCrossRefGoogle Scholar
  95. Holland S, Lodwig E, Sideri T, Reader T, Clarke I, Gkargkas K, Hoyle DC, Delneri D, Oliver SG, Avery SV (2007) Application of the comprehensive set of heterozygous yeast deletion mutants to elucidate the molecular basis of cellular chromium toxicity. Genome Biol 8:R268CrossRefGoogle Scholar
  96. Hong-Bo S, Li-Ye C, Cheng-Jiang R, Hua L, Dong-Gang G, Wei-Xiang L (2010) Understanding molecular mechanisms for improving phytoremediation of heavy metal-contaminated soils. Crit Rev Biotechnol 30:23–30PubMedCrossRefGoogle Scholar
  97. Hosiner D, Lempiäinen H, Reiter W, Urban J, Loewith R, Ammerer G, Schweyen R, Shore D, Schüller C (2009) Arsenic toxicity to Saccharomyces cerevisiae is a consequence of inhibition of the TORC1 kinase combined with a chronic stress response. Mol Biol Cell 20:1048–1057PubMedCrossRefGoogle Scholar
  98. Hwang GW, Furuchi T, Naganuma A (2007) Ubiquitin-conjugating enzyme Cdc34 mediates cadmium resistance in budding yeast through ubiquitination of the transcription factor Met4. Biochem Biophys Res Commun 363:873–878PubMedCrossRefGoogle Scholar
  99. Jarosz-Wilkołazka A, Gadd GM (2003) Oxalate production by wood-rotting fungi growing in toxic metal-amended medium. Chemosphere 52:541–547PubMedCrossRefGoogle Scholar
  100. Jarosz-Wilkołazka A, Graz M, Braha B, Menge S, Schlosser D, Krauss GJ (2006) Species-specific Cd-stress response in the white rot basidiomycetes Abortiporus biennis and Cerrena unicolor. Biometals 19:39–49PubMedCrossRefGoogle Scholar
  101. Jin YH, Dunlap PE, McBride SJ, Al-Refai H, Bushel PR, Freedman JH (2008) Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet 4:e1000053CrossRefGoogle Scholar
  102. Jo WJ, Loguinov A, Chang M, Wintz H, Nislow C, Arkin AP, Giaever G, Vulpe CD (2008) Identification of genes involved in the toxic response of Saccharomyces cerevisiae against iron and copper overload by parallel analysis of deletion mutants. Toxicol Sci 101:140–151PubMedCrossRefGoogle Scholar
  103. Johnson L (2008) Iron and siderophores in fungal-host interactions. Mycol Res 112:170–183PubMedCrossRefGoogle Scholar
  104. Kakimoto M, Kobayashi A, Fukuda R, Ono Y, Ohta A, Yoshimura E (2005) Genome-wide screening of aluminum tolerance in Saccharomyces cerevisiae. Biometals 18:467–474PubMedCrossRefGoogle Scholar
  105. Kanamasa S, Sumi K, Yamuki N, Kumasaka T, Miura T, Abe F, Kajiwara S (2007) Cloning and functional characterization of the copper/zinc superoxide dismutase gene from the heavy-metal-tolerant yeast Cryptococcus liquefaciens strain N6. Mol Genet Genomics 277:403–412PubMedCrossRefGoogle Scholar
  106. Kang SH, Bozhilov KN, Myung NV, Mulchandani A, Chen W (2008) Microbial synthesis of CdS nanocrystals in genetically engineered E. coli. Angew Chem. Int Ed Engl 47:5186–5189PubMedCrossRefGoogle Scholar
  107. Katsifas EA, Giannoutsou E, Lambraki M, Barla M, Karagouni AD (2004) Chromium recycling of tannery waste through microbial fermentation. J Ind Microbiol Biotechnol 31:57–62PubMedCrossRefGoogle Scholar
  108. Kennedy PJ, Vashisht AA, Hoe KL, Kim DU, Park HO, Hayles J, Russell P (2008) A genome-wide screen of genes involved in cadmium tolerance in Schizosaccharomyces pombe. Toxicol Sci 106:124–139PubMedCrossRefGoogle Scholar
  109. 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 18:355–364PubMedCrossRefGoogle Scholar
  110. Koósz Z, Gazdag Z, Miklós I, Benko Z, Belágyi J, Antal J, Meleg B, Pesti M (2008) Effects of decreased specific glutathione reductase activity in a chromate-tolerant mutant of Schizosaccharomyces pombe. Folia Microbiol 53:308–314CrossRefGoogle Scholar
  111. Kowshik M, Deshmukh N, Vogel W, Urban J, Kulkarni SK, Paknikar KM (2002) Microbial synthesis of semiconductor CdS nanoparticles, their characterization, and their use in the fabrication of an ideal diode. Biotechnol Bioeng 78:583–588PubMedCrossRefGoogle Scholar
  112. Krznaric E, Verbruggen N, Wevers JH, Carleer R, Vangronsveld J, Colpaert JV (2009) Cd-tolerant Suillus luteus: a fungal insurance for pines exposed to Cd. Environ Pollut 157:1581–1588PubMedCrossRefGoogle Scholar
  113. Kumar KS, Dayananda S, Subramanyam C (2005) Copper alone, but not oxidative stress, induces copper-metallothionein gene in Neurospora crassa. FEMS Microbiol Lett 242:45–50PubMedCrossRefGoogle Scholar
  114. Kunstmann B, Osiewacz HD (2009) The S-adenosylmethionine dependent O-methyltransferase PaMTH1: a longevity assurance factor protecting Podospora anserina against oxidative stress. Aging (Albany NY) 1:328–334Google Scholar
  115. Kuroda K, Ueda M (2010) Engineering of microorganisms towards recovery of rare metal ions. Appl Microbiol Biotechnol 87:53–60PubMedCrossRefGoogle Scholar
  116. Lanfranco L, Balsamo R, Martino E, Perotto S, Bonfante P (2002a) Zinc ions alter morphology and chitin deposition in an ericoid fungus. Eur J Histochem 46:341–350Google Scholar
  117. Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002b) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67CrossRefGoogle Scholar
  118. Lanfranco L, Balsamo R, Martino E, Bonfante P, Perotto S (2004) Zinc ions differentially affect chitin synthase gene expression in an ericoid mycorrhizal fungus. Plant Biosyst 138:271–277CrossRefGoogle Scholar
  119. Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Environ Qual 31:109–120PubMedCrossRefGoogle Scholar
  120. Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522PubMedCrossRefGoogle Scholar
  121. Lewinska A, Bartosz G (2007) Protection of yeast lacking the Ure2 protein against the toxicity of heavy metals and hydroperoxides by antioxidants. Free Radic Res 41:580–590PubMedCrossRefGoogle Scholar
  122. Li L, Chen OS, McVey Ward D, Kaplan J (2001) CCC1 is a transporter that mediates vacuolar iron storage in yeast. J Biol Chem 276:29515–29519PubMedCrossRefGoogle Scholar
  123. Li L, Bagley D, Ward DM, Kaplan J (2008) Yap5 is an iron-responsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol Cell Biol 28:1326–1337PubMedCrossRefGoogle Scholar
  124. Liang Q, Zhou B (2007) Copper and manganese induce yeast apoptosis via different pathways. Mol Biol Cell 18:4741–4749PubMedCrossRefGoogle Scholar
  125. Liu XF, Culotta VC (1999) Post-translation control of Nramp metal transport in yeast. Role of metal ions and the BSD2 gene. J Biol Chem 274:4863–4868PubMedCrossRefGoogle Scholar
  126. Liu XF, Supek F, Nelson N, Culotta VC (1997) Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene. J Biol Chem 272:11763–11769PubMedCrossRefGoogle Scholar
  127. Lyons TJ, Gasch AP, Gaitherm LA, Botstein D, Brown PO, Eide DJ (2000) Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc Natl Acad Sci U S A 97:7957–7962PubMedCrossRefGoogle Scholar
  128. Lyons TJ, Villa NY, Regalla LM, Kupchak BR, Vagstad A, Eide DJ (2004) Metalloregulation of yeast membrane steroid receptor homologs. Proc Natl Acad Sci U S A 101:5506–5511PubMedCrossRefGoogle Scholar
  129. MacDiarmid CW, Gaither LA, Eide D (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19:2845–2855PubMedCrossRefGoogle Scholar
  130. Maciaszczyk-Dziubinska E, Migdal I, Migocka M, Bocer T, Wysocki R (2010) The yeast aquaglyceroporin Fps1p is a bidirectional arsenite channel. FEBS Lett 584:726–732PubMedCrossRefGoogle Scholar
  131. Maheswari S, Murugesan AG (2009) Remediation of arsenic in soil by Aspergillus nidulans isolated from an arsenic-contaminated site. Environ Technol 30:921–926PubMedCrossRefGoogle Scholar
  132. Mai C, Kües U, Militz H (2004) Biotechnology in the wood industry. Appl Microbiol Biotechnol 63:477–494PubMedCrossRefGoogle Scholar
  133. Mannazzu I, Guerra E, Ferretti R, Pediconi D, Fatichenti F (2000) Vanadate and copper induce overlapping oxidative stress responses in the vanadate-tolerant yeast Hansenula polymorpha. Biochim Biophys Acta 1475:151–156PubMedCrossRefGoogle Scholar
  134. Marion RM, Regev A, Segal E, Barash Y, Koller D, Friedman N, O’Shea EK (2004) Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. Proc Natl Acad Sci U S A 101:14315–14322PubMedCrossRefGoogle Scholar
  135. Marques AP, Rangel AO, Castro PM (2009) Remediation of heavy metal contaminated soils: phytoremediation as a potentially promising clean-up technology. Crit Rev Environ Sci Technol 39:622–654CrossRefGoogle Scholar
  136. Medicherla B, Goldberg AL (2008) Heat shock and oxygen radicals stimulate ubiquitin-dependent degradation mainly of newly synthesized proteins. J Cell Biol 182:663–673PubMedCrossRefGoogle Scholar
  137. Mejáre M, Bülow L (2001) Metal-binding proteins and peptides in bioremediation and phytoremediation of heavy metals. Trends Biotechnol 19:67–73PubMedCrossRefGoogle Scholar
  138. Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671PubMedCrossRefGoogle Scholar
  139. Migdal I, Ilina Y, Tamás MJ, Wysocki R (2008) Mitogen-activated protein kinase Hog1 mediates adaptation to G1 checkpoint arrest during arsenite and hyperosmotic stress. Eukaryot Cell 7:1309–1317PubMedCrossRefGoogle Scholar
  140. Miskei M, Karányi Z, Pócsi I (2009) Annotation of stress-response proteins in the aspergilli. Fungal Genet Biol 46:S105–S120PubMedCrossRefGoogle Scholar
  141. Momose Y, Iwahashi H (2001) Bioassay of cadmium using a DNA microarray: genome-wide expression patterns of Saccharomyces cerevisiae response to cadmium. Environ Toxicol Chem 20:2353–2360PubMedGoogle Scholar
  142. More TT, Yan S, Tyagi RD, Surampalli RY (2010) Potential use of filamentous fungi for wastewater sludge treatment. Bioresour Technol 101:7691–7700CrossRefGoogle Scholar
  143. Mukherjee A, Das D, Kumar Mondal S, Biswas R, Kumar Das T, Boujedaini N, Khuda-Bukhsh AR (2010) Tolerance of arsenate-induced stress in Aspergillus niger, a possible candidate for bioremediation. Ecotoxicol Environ Saf 73:172–182PubMedCrossRefGoogle Scholar
  144. Muller LA, Craciun AR, Ruytinx J, Lambaerts M, Verbruggen N, Vangronsveld J, Colpaert JV (2007) Gene expression profiling of a Zn-tolerant and a Zn-sensitive Suillus luteus isolate exposed to increased external zinc concentrations. Mycorrhiza 17:571–580PubMedCrossRefGoogle Scholar
  145. Mulligan CN, Kamali M, Gibbs BF (2004) Bioleaching of heavy metals from a low-grade mining ore using Aspergillus niger. J Hazard Mater 110:77–84PubMedCrossRefGoogle Scholar
  146. Nagy Z, Montigny C, Leverrier P, Yeh S, Goffeau A, Garrigos M, Falson P (2006) Role of the yeast ABC transporter Yor1p in cadmium detoxification. Biochimie 88:1665–1671PubMedCrossRefGoogle Scholar
  147. Nargund AM, Avery SV, Houghton JE (2008) Cadmium induces a heterogeneous and caspase-dependent apoptotic response in Saccharomyces cerevisiae. Apoptosis 13:811–821PubMedCrossRefGoogle Scholar
  148. Oddon DM, Diatloff E, Roberts SK (2007) A CLC chloride channel plays an essential role in copper homeostasis in Aspergillus nidulans at increased extracellular copper concentrations. Biochim Biophys Acta 1768:2466–2477PubMedCrossRefGoogle Scholar
  149. Ono BI, Ishii N, Fujino S, Aoyama I (1991) Role of hydrosulfide ions (HS-) in methylmercury resistance in Saccharomyces cerevisiae. Appl Environ Microbiol 57:3183–3186Google Scholar
  150. Orłowska E, Mesjasz-Przybyłowicz J, Przybyłowicz W, Turnau K (2008) Nuclear microprobe studies of elemental distribution in mycorrhizal and non-mycorrhizal roots of Ni-hyperaccumulator Berkheya coddii. XRay Spectom 37:129–132CrossRefGoogle Scholar
  151. Ortiz DF, Ruscitti T, McCue KF, Ow DW (1995) Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J Biol Chem 270:4721–4728PubMedCrossRefGoogle Scholar
  152. Osaki Y, Shirabe T, Tamura S, Yoshimura E (2008) A functional putative phytochelatin synthase from the primitive red alga Cyanidioschyzon merolae. Biosci Biotechnol Biochem 72:3306–3309PubMedCrossRefGoogle Scholar
  153. Ott T, Fritz E, Polle A, Schützendübel A (2002) Characterisation of antioxidative systems in the ectomycorrhiza-building basidiomycete Paxillus involutus (Bartsch) Fr. and its reaction to cadmium. FEMS Microbiol Ecol 42:359–366PubMedCrossRefGoogle Scholar
  154. 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 162:634–649PubMedCrossRefGoogle Scholar
  155. Pagani MA, Casamayor A, Serrano R, Atrian S, Ariño J (2007) Disruption of iron homeostasis in Saccharomyces cerevisiae by high zinc levels: a genome-wide study. Mol Microbiol 65:521–537PubMedCrossRefGoogle Scholar
  156. 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 171:761–766Google Scholar
  157. Paraszkiewicz K, Długoński J (2009) Effect of nickel, copper, and zinc on emulsifier production and saturation of cellular fatty acids in the filamentous fungus Curvularia lunata. Int Biodeter Biodegr 63:100–105CrossRefGoogle Scholar
  158. Paraszkiewicz K, Frycie A, Słaba M, Długoński J (2007) Enhancement of emulsifier production by Curvularia lunata in cadmium, zinc and lead presence. Biometals 20:797–805PubMedCrossRefGoogle Scholar
  159. Paraszkiewicz K, Bernat P, Naliwajski M, Długoński J (2010) Lipid peroxidation in the fungus Curvularia lunata exposed to nickel. Arch Microbiol 192:135–141PubMedCrossRefGoogle Scholar
  160. Pereira Y, Lagniel G, Godat E, Baudouin-Cornu P, Junot C, Labarre J (2008) Chromate causes sulfur starvation in yeast. Toxicol Sci 106:400–412PubMedCrossRefGoogle Scholar
  161. Perrone GG, Grant CM, Dawes IW (2005) Genetic and environmental factors influencing GSH homeostasis in Saccharomyces cerevisiae. Mol Biol Cell 16:218–230PubMedCrossRefGoogle Scholar
  162. Pesti M, Gazdag Z, Emri T, Farkas N, Koósz Z, Belágyi J, Pócsi I (2002) Chromate sensitivity in fission yeast is caused by increased glutathione reductase activity and peroxide overproduction. J Basic Microbiol 42:408–419PubMedCrossRefGoogle Scholar
  163. Pinson B, Sagot I, Daignan-Fornier B (2000) Identification of genes affecting selenite toxicity and resistance in Saccharomyces cerevisiae. Mol Microbiol 36:679–687PubMedCrossRefGoogle Scholar
  164. Pócsi I, Prade RA, Penninckx MJ (2004) GSH, altruistic metabolite in fungi. Adv Microb Physiol 49:1–76PubMedCrossRefGoogle Scholar
  165. Pócsi I, Miskei M, Karányi Z, Emri T, Ayoubi P, Pusztahelyi T, Balla G, Prade RA (2005) Comparison of gene expression signatures of diamide, H2O2 and menadione exposed Aspergillus nidulans cultures-linking genome-wide transcriptional changes to cellular physiology. BMC Genomics 6:182PubMedCrossRefGoogle Scholar
  166. Pócsi I, Jeney V, Kertai P, Pócsi I, Emri T, Gyémánt G, Fésüs L, Balla J, Balla G (2008) Fungal siderophores function as protective agents of LDL oxidation and are promising anti-atherosclerotic metabolites in functional food. Mol Nutr Food Res 52:1434–1447PubMedCrossRefGoogle Scholar
  167. Poljšak B, Gazdag Z, Jenko-Brinovec Š, Fujs Š, Pesti M, Bélagyi J, Plesničar S, Raspor P (2005) Pro-oxidative vs antioxidative properties of ascorbic acid in chromium(VI)-induced damage: an in vivo and in vitro approach. J Appl Toxicol 25:535–548PubMedCrossRefGoogle Scholar
  168. Poljšak B, Pócsi I, Raspor P, Pesti M (2010) Interference of chromium with biological systems in yeasts and fungi: a review. J Basic Microbiol 50:21–36PubMedCrossRefGoogle Scholar
  169. Portnoy ME, Liu XF, Culotta VC (2000) Saccharomyces cerevisiae expresses three functionally distinct homologues of the nramp family of metal transporters. Mol Cell Biol 20:7893–7902PubMedCrossRefGoogle Scholar
  170. Prasad K, Jham AK (2010) Biosynthesis of CdS nanoparticles: an improved green and rapid procedure. J Colloid Interface Sci 342:68–72PubMedCrossRefGoogle Scholar
  171. Prévéral S, Gayet L, Moldes C, Hoffmann J, Mounicou S, Gruet A, Reynaud F, Lobinski R, Verbavatz JM, Vavasseur A, Forestier C (2009) A common highly conserved cadmium detoxification mechanism from bacteria to humans: heavy metal tolerance conferred by the ATP-binding cassette (ABC) transporter SpHMT1 requires GSH but not metal-chelating phytochelatin peptides. J Biol Chem 284:4936–4943PubMedCrossRefGoogle Scholar
  172. Price MS, Classen JJ, Payne GA (2001) Aspergillus niger absorbs copper and zinc from swine wastewater. Bioresour Technol 77:41–49PubMedCrossRefGoogle Scholar
  173. Purakayastha TJ, Chhonkar PK (2010) Phytoremediation of heavy metal contaminated soils. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Berlin, pp 389–429CrossRefGoogle Scholar
  174. Purin S, Rillig MC (2008) Immuno-cytolocalization of glomalin in the mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. Soil Biol Biochem 40:1000–1003CrossRefGoogle Scholar
  175. Pynyaha YV, Boretskym YR, Fedorovych DV, Fayura LR, Levkiv AI, Ubiyvovk VM, Protchenko OV, Philpott CC, Sibirny AA (2010) Deficiency in frataxin homologue YFH1 in the yeast Pichia guilliermondii leads to missregulation of iron acquisition and riboflavin biosynthesis and affects sulfate assimilation. Biometals 22:1051–1061Google Scholar
  176. Rajendran P, Ashokkumar B, Muthukrishnan J, Gunasekaran P (2002) Toxicity assessment of nickel using Aspergillus niger and its removal from an industrial effluent. Appl Biochem Biotechnol 102–103:201–206Google Scholar
  177. Ramesh G, Podila GK, Gay G, Marmeisse R, Reddy MS (2009) Different patterns of regulation for the copper and cadmium metallothioneins of the ectomycorrhizal fungus Hebeloma cylindrosporum. Appl Environ Microbiol 75:2266–2274Google Scholar
  178. Ramos J, Clemente MR, Naya L, Loscos J, Pérez-Rontomé C, Sato S, Tabata S, Becana M (2007) Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol 143:1110–1118PubMedCrossRefGoogle Scholar
  179. Rea PA, Vatamaniuk OK, Rigden DJ (2004) Weeds, worms, and more. Papain’s long-lost cousin, phytochelatin synthase. Plant Physiol 136:2463–2474PubMedCrossRefGoogle Scholar
  180. Rees EM, Lee J, Thiele DJ (2004) Mobilization of intracellular copper stores by the ctr2 vacuolar copper transporter. J Biol Chem 279:54221–54229PubMedCrossRefGoogle Scholar
  181. Reisinger S, Schiavon M, Terry N, Pilon-Smits EA (2008) Heavy metal tolerance and accumulation in Indian mustard (Brassica juncea L.) expressing bacterial γ-glutamylcysteine synthetase or glutathione synthetase. Int J Phytoremediation 10:440–454PubMedCrossRefGoogle Scholar
  182. Ren WX, Li PJ, Geng Y, Li XJ (2009) Biological leaching of heavy metals from a contaminated soil by Aspergillus niger. J Hazard Mater 167:164–169PubMedCrossRefGoogle Scholar
  183. Rodrigues-Pousada C, Menezes RA, Pimentel C (2010) The Yap family and its role in stress response. Yeast 27:245–258PubMedCrossRefGoogle Scholar
  184. Ruotolo R, Marchini G, Ottonello S (2008) Membrane transporters and protein traffic networks differentially affecting metal tolerance: a genomic phenotyping study in yeast. Genome Biol 9:R67CrossRefGoogle Scholar
  185. Salin H, Fardeau V, Piccini E, Lelandais G, Tanty V, Lemoine S, Jacq C, Devaux F (2008) Structure and properties of transcriptional networks driving selenite stress response in yeasts. BMC Genomics 9:333PubMedCrossRefGoogle Scholar
  186. Sandana Mala JG, Unni Nair B, Puvanakrishnan R (2006) Bioaccumulation and biosorption of chromium by Aspergillus niger MTCC 2594. J Gen Appl Microbiol 52:179–186PubMedCrossRefGoogle Scholar
  187. Sankaran S, Khanal SK, Jasti N, Jin B, Pometto III AL, Van Leeuwen JH (2010) Use of filamentous fungi for wastewater treatment and production of high value fungal byproducts: a review. Crit Rev Environ Sci Technol 40:400–449CrossRefGoogle Scholar
  188. Scheckhuber CQ, Mitterbauer R, Osiewacz HD (2009) Molecular basis of and interference into degenerative processes in fungi: potential relevance for improving biotechnological performance of microorganisms. Appl Microbiol Biotechnol 85:27–35PubMedCrossRefGoogle Scholar
  189. Schlosser D, Höfer C (2002) Laccase-catalyzed oxidation of Mn2+ in the presence of natural Mn3+ chelators as a novel source of extracellular H2O2 production and its impact on manganese peroxidase. Appl Environ Microbiol 68:3514–3521PubMedCrossRefGoogle Scholar
  190. Schrettl M, Bignell E, Kragl C, Sabiha Y, Loss O, Eisendle M, Wallner A, Arst HN Jr, Haynes K, Haas H (2007) Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog 3:1195–1207PubMedCrossRefGoogle Scholar
  191. Schrettl M, Kim HS, Eisendle M, Kragl C, Nierman WC, Heinekamp T, Werner ER, Jacobsen I, Illmer P, Yi H, Brakhage AA, Haas H (2008) SreA-mediated iron regulation in Aspergillus fumigatus. Mol Microbiol 70:27–43PubMedCrossRefGoogle Scholar
  192. Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365PubMedCrossRefGoogle Scholar
  193. Seguin A, Bayot A, Dancis A, Rogowska-Wrzesinska A, Auchère F, Camadro JM, Bulteau AL, Lesuisse E (2009) Overexpression of the yeast frataxin homolog (Yfh1): contrasting effects on iron-sulfur cluster assembly, heme synthesis and resistance to oxidative stress. Mitochondrion 9:130–138PubMedCrossRefGoogle Scholar
  194. Seguin A, Sutak R, Bulteau AL, Garcia-Serres R, Oddou JL, Lefevre S, Santos R, Dancis A, Camadro JM, Latour JM, Lesuisse E (2010) Evidence that yeast frataxin is not an iron storage protein in vivo. Biochim Biophys Acta 1802:531–538PubMedCrossRefGoogle Scholar
  195. Serero A, Lopes J, Nicolas A, Boiteux S (2008) Yeast genes involved in cadmium tolerance: identification of DNA replication as a target of cadmium toxicity. DNA Repair (Amst) 7:1262–1275CrossRefGoogle Scholar
  196. Shakoury-Elizeh M, Tiedeman J, Rashford J, Ferea T, Demeter J, Garcia E, Rolfes R, Brown PO, Botstein D, Philpott CC (2004) Transcriptional remodeling in response to iron deprivation in Saccharomyces cerevisiae. Mol Biol Cell 15:1233–1243PubMedCrossRefGoogle Scholar
  197. Shakoury-Elizeh M, Protchenko O, Berger A, Cox J, Gable K, Dunn TM, Prinz WA, Bard M, Philpott CC (2010) Metabolic response to iron deficiency in Saccharomyces cerevisiae. J Biol Chem 285:14823–14833PubMedCrossRefGoogle Scholar
  198. Sharma KG, Mason DL, Liu G, Rea PA, Bachhawat AK, Michaelis S (2002) Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter. Eukaryot Cell 1:391–400PubMedCrossRefGoogle Scholar
  199. Sharma S, Malik A, Satya S (2009) Application of response surface methodology (RSM) for optimization of nutrient supplementation for Cr (VI) removal by Aspergillus lentulus AML05. J Hazard Mater 164:1198–1204PubMedCrossRefGoogle Scholar
  200. Sheoran V, Sheoran AS, Poonia P (2009) Phytomining: A review. Minerals Eng 22:1007–1019CrossRefGoogle Scholar
  201. Sierra-Alvarez R (2007) Fungal bioleaching of metals in preservative-treated wood. Proc Biochem 42:798–804CrossRefGoogle Scholar
  202. Sierra-Alvarez R (2009) Removal of copper, chromium and arsenic from preservative-treated wood by chemical extraction-fungal bioleaching. Waste Manag 29:1885–1891PubMedCrossRefGoogle Scholar
  203. Simate GS, Ndlovu S, Walubita LF (2010) The fungal and chemolithotrophic leaching of nickel laterites—challenges and opportunities. Hydrometallurgy 103:150–157CrossRefGoogle Scholar
  204. Song WY, Sohn EJ, Martinoia E, Lee YJ, Yang YY, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21:914–919PubMedCrossRefGoogle Scholar
  205. Srikanth CV, Vats P, Bourbouloux A, Delrot S, Bachhawat AK (2005) Multiple cis-regulatory elements and the yeast sulphur regulatory network are required for the regulation of the yeast GSH transporter, Hgt1p. Curr Genet 47:345–358PubMedCrossRefGoogle Scholar
  206. Srinivasan C, Liba A, Imlay JA, Valentine JS, Gralla EB (2000) Yeast lacking superoxide dismutase(s) show elevated levels of “free iron” as measured by whole cell electron paramagnetic resonance. J Biol Chem 275:29187–29192PubMedCrossRefGoogle Scholar
  207. Srivastava S, Thakur IS (2006) Isolation and process parameter optimization of Aspergillus sp. for removal of chromium from tannery effluent. Bioresour Technol 97:1167–1173PubMedCrossRefGoogle Scholar
  208. Stadler JA, Schweyen RJ (2002) The yeast iron regulon is induced upon cobalt stress and crucial for cobalt tolerance. J Biol Chem 277:39649–39654PubMedCrossRefGoogle Scholar
  209. Stephen DW, Jamieson DJ (1997) Amino acid-dependent regulation of the Saccharomyces cerevisiae GSH1 gene by hydrogen peroxide. Mol Microbiol 23:203–210PubMedCrossRefGoogle Scholar
  210. Stroobants A, Delroisse JM, Delvigne F, Delva J, Portetelle D, Vandenbol M (2009) Isolation and biomass production of a Saccharomyces cerevisiae strain binding copper and zinc ions. Appl Biochem Biotechnol 157:85–97PubMedCrossRefGoogle Scholar
  211. Sumner ER, Shanmuganathan A, Sideri TC, Willetts SA, Houghton JE, Avery SV (2005) Oxidative protein damage causes chromium toxicity in yeast. Microbiology 151:1939–1948PubMedCrossRefGoogle Scholar
  212. Sun YM, Horng CY, Chang FL, Cheng LC, Tian WX (2010) Biosorption of lead, mercury, and cadmium ions by Aspergillus terreus immobilized in a natural matrix. Pol J Microbiol 59:37–44PubMedGoogle Scholar
  213. Swami D, Buddhi D (2006) Removal of contaminants from industrial wastewater through various non-conventional technologies: a review. Int J Environ Pollut 27:324–346Google Scholar
  214. Tamás MJ, Labarre J, Toledano MB, Wysocki R (2005) Mechanisms of toxic metal tolerance in yeast. In: Tamás MJ, Martinoia E (eds) Molecular biology of metal homeostasis and detoxification: from microbes to man. Springer, Heidelberg, pp 395–454Google Scholar
  215. Taştan BE, Ertuğrul S, Dönmez G (2010) Effective bioremoval of reactive dye and heavy metals by Aspergillus versicolor. Bioresour Technol 101:870–876PubMedCrossRefGoogle Scholar
  216. Thomas JC, Davies EC, Malick FK, Endreszl C, Williams CR, Abbas M, Petrella S, Swisher K, Perron M, Edwards R, Osenkowski P, Urbanczyk N, Wiesend WN, Murray KS (2003) Yeast metallothionein in transgenic tobacco promotes copper uptake from contaminated soils. Biotechnol Prog 19:273–280Google Scholar
  217. Thorsen M, Di Y, Tängemo C, Morillas M, Ahmadpour D, Van der Does C, Wagner A, Johansson E, Boman J, Posas F, Wysocki R, Tamás MJ (2006) The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol Biol Cell 17:4400–4410PubMedCrossRefGoogle Scholar
  218. Thorsen M, Lagniel G, Kristiansson E, Junot C, Nerman O, Labarre J, Tamás MJ (2007) Quantitative transcriptome, proteome, and sulfur metabolite profiling of the Saccharomyces cerevisiae response to arsenite. Physiol Genomics 30:35–43PubMedCrossRefGoogle Scholar
  219. Thorsen M, Perrone GG, Kristiansson E, Traini M, Ye T, Dawes IW, Nerman O, Tamás MJ (2009) Genetic basis of arsenite and cadmium tolerance in Saccharomyces cerevisiae. BMC Genomics 10:105PubMedCrossRefGoogle Scholar
  220. Todorova D, Nedeva D, Abrashev R, Tsekova K (2008) Cd(II) stress response during the growth of Aspergillus niger B 77. J Appl Microbiol 104:178–184PubMedGoogle Scholar
  221. Tóth V, Antal K, Gyémánt G, Miskei M, Pócsi I, Emri T (2009) Optimization of coprogen production in Neurospora crassa. Acta Biol Hung 60:321–328PubMedCrossRefGoogle Scholar
  222. Urbanowski JL, Piper RC (1999) The iron transporter Fth1p forms a complex with the Fet5 iron oxidase and resides on the vacuolar membrane. J Biol Chem 274:38061–38070PubMedCrossRefGoogle Scholar
  223. Vallino M, Martino E, Boella F, Murat C, Chiapello M, Perotto S (2009) Cu,Zn superoxide dismutase and zinc stress in the metal-tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn. FEMS Microbiol Lett 293:48–57PubMedCrossRefGoogle Scholar
  224. Vashisht AA, Kennedy PJ, Russell P (2009) Centaurin-like protein Cnt5 contributes to arsenic and cadmium resistance in fission yeast. FEMS Yeast Res 9:257–269PubMedCrossRefGoogle Scholar
  225. Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals. Phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J Biol Chem 276:20817–20820PubMedCrossRefGoogle Scholar
  226. Verma VC, Kharwar RN, Gange AC (2010) Biosynthesis of antimicrobial silver nanoparticles by the endophytic fungus Aspergillus clavatus. Nanomedicine (Lond) 5:33–40CrossRefGoogle Scholar
  227. Vesentini D, Dickinson DJ, Murphy RJ (2006) Fungicides affect the production of fungal extracellular mucilaginous material (ECMM) and the peripheral growth unit (PGU) in two wood-rotting basidiomycetes. Mycol Res 110:1207–1213PubMedCrossRefGoogle Scholar
  228. Vido K, Spector D, Lagniel G, Lopez S, Toledano MB, Labarre J (2001) A proteome analysis of the cadmium response in Saccharomyces cerevisiae. J Biol Chem 276:8469–8474PubMedCrossRefGoogle Scholar
  229. Villegas LB, Amoroso MJ, de Figueroa LI, Siñeriz F, Siñeriz F (2009) Cu(II) removal by Rhodotorula mucilaginosa RCL-11 in sequential batch cultures. Water Sci Technol 60:1225–1232PubMedCrossRefGoogle Scholar
  230. Wang J, Chen C (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol Adv 24:427–451PubMedCrossRefGoogle Scholar
  231. Wang ZY, He XP, Zhang BR (2007) Over-expression of GSH1 gene and disruption of PEP4 gene in self-cloning industrial brewer’s yeast. Int J Food Microbiol 119:192–199PubMedCrossRefGoogle Scholar
  232. Wang ZY, Wang JJ, Liu XF, He XP, Zhang BR (2009) Recombinant industrial brewing yeast strains with ADH2 interruption using self-cloning GSH1+CUP1 cassette. FEMS Yeast Res 9:574–581PubMedCrossRefGoogle Scholar
  233. Wang X, Xu H, Ha SW, Ju D, Xie Y (2010) Proteasomal degradation of Rpn4 in Saccharomyces cerevisiae is critical for cell viability under stressed conditions. Genetics 184:335–342PubMedCrossRefGoogle Scholar
  234. Warmka J, Hanneman J, Lee J, Amin D, Ota I (2001) Ptc1, a type 2C Ser/Thr phosphatase, inactivates the HOG pathway by dephosphorylating the mitogen-activated protein kinase Hog1. Mol Cell Biol 21:51–60PubMedCrossRefGoogle Scholar
  235. Wawrzyński A, Kopera E, Wawrzyńska A, Kamińska J, Bal W, Sirko A (2006) Effects of simultaneous expression of heterologous genes involved in phytochelatin biosynthesis on thiol content and cadmium accumulation in tobacco plants. J Exp Bot 57:2173–2182PubMedCrossRefGoogle Scholar
  236. Weiersbye IM, Straker CJ, Przybylowicz WJ (1999) Micro-PIXE mapping of elemental distribution in arbuscular mycorrhizal roots of the grass, Cynodon dactylon, from gold and uranium mine tailings. Nucl Instrum Merhods Phys Res Sec B 158:335–343CrossRefGoogle Scholar
  237. Wemmie JA, Szczypka MS, Thiele DJ, Moye-Rowley WS (1994) Cadmium tolerance mediated by the yeast AP-1 protein requires the presence of an ATP-binding cassette transporter-encoding gene, YCF1. J Biol Chem 269:32592–32597PubMedGoogle Scholar
  238. Westwater J, McLaren NF, Dormer UH, Jamieson DJ (2002) The adaptive response of Saccharomyces cerevisiae to mercury exposure. Yeast 19:233–239PubMedCrossRefGoogle Scholar
  239. Wright SF, Franke-Snyder M, Morton JB, Upadhyaya A (1996) Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant Soil 181:193–203CrossRefGoogle Scholar
  240. Wu AL, Moye-Rowley WS (1994) GSH1, which encodes γ-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol Cell Biol 14:5832–5839PubMedCrossRefGoogle Scholar
  241. Wu CY, Bird AJ, Chung LM, Newton MA, Winge DR, Eide DJ (2008) Differential control of Zap1-regulated genes in response to zinc deficiency in Saccharomyces cerevisiae. BMC Genomics 9:370PubMedCrossRefGoogle Scholar
  242. Wu G, Kang H, Zhang X, Shao H, Chu L, Ruan C (2010) A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities. J Hazard Mater 174:1–8PubMedCrossRefGoogle Scholar
  243. Wurgler-Murphy SM, Maeda T, Witten EA, Saito H (1997) Regulation of the Saccharomyces cerevisiae HOG1 mitogen-activated protein kinase by the PTP2 and PTP3 protein tyrosine phosphatases. Mol Cell Biol 17:1289–1297PubMedGoogle Scholar
  244. Wysocki R, Tamás MJ (2010) How Saccharomyces cerevisiae copes with toxic metals and metalloids. FEMS Microbiol Rev 34:925–951Google Scholar
  245. Wysocki R, Bobrowicz P, Ułaszewski S (1997) The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J Biol Chem 272:30061–30066PubMedCrossRefGoogle Scholar
  246. Wysocki R, Chéry CC, Wawrzycka D, Van Hulle M, Cornelis R, Thevelein JM, Tamás MJ (2001) The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol Microbiol 40:1391–1401PubMedCrossRefGoogle Scholar
  247. Wysocki R, Clemens S, Augustyniak D, Golik P, Maciaszczyk E, Tamás MJ, Dziadkowiec D (2003) Metalloid tolerance based on phytochelatins is not functionally equivalent to the arsenite transporter Acr3p. Biochem Biophys Res Commun 304:293–300PubMedCrossRefGoogle Scholar
  248. Wysocki R, Fortier PK, Maciaszczyk E, Thorsen M, Leduc A, Odhagen A, Owsianik G, Ulaszewski S, Ramotar D, Tamás MJ (2004) Transcriptional activation of metalloid tolerance genes in Saccharomyces cerevisiae requires the AP-1-like proteins Yap1p and Yap8p. Mol Biol Cell 15:2049–2060PubMedCrossRefGoogle Scholar
  249. Yamaguchi-Iwai Y, Dancis A, Klausner RD (1995) AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J 14:1231–1239PubMedGoogle Scholar
  250. Yang HC, Pon LA (2003) Toxicity of metal ions used in dental alloys: a study in the yeast Saccharomyces cerevisiae. Drug Chem Toxicol 26:75–85PubMedCrossRefGoogle Scholar
  251. Yasokawa D, Murata S, Kitagawa E, Iwahashi Y, Nakagawa R, Hashido T, Iwahashi H (2008) Mechanisms of copper toxicity in Saccharomyces cerevisiae determined by microarray analysis. Environ Toxicol 23:599–606PubMedCrossRefGoogle Scholar
  252. Yompakdee C, Bun-ya M, Shikata K, Ogawa N, Harashima S, Oshima Y (1996) A putative new membrane protein, Pho86p, in the inorganic phosphate uptake system of Saccharomyces cerevisiae. Gene 171:41–47PubMedCrossRefGoogle Scholar
  253. Zhang B, Georgiev O, Hagmann M, Günes C, Cramer M, Faller P, Vasák M, Schaffner W (2003) Activity of metal-responsive transcription factor 1 by toxic heavy metals and H2O2 in vitro is modulated by metallothionein. Mol Cell Biol 23:8471–8485PubMedCrossRefGoogle Scholar
  254. Zhou S, Fushinobu S, Kim SW, Nakanishim Y, Wakagi T, Shoun H (2010) Aspergillus oryzae flavohemoglobins promote oxidative damage by hydrogen peroxide. Biochem Biophys Res Commun 394:558–561PubMedCrossRefGoogle Scholar
  255. Zhu YL, Pilon-Smits EA, Jouanin L, Terry N (1999a) Overexpression of glutathione synthetase in indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119:73–80CrossRefGoogle Scholar
  256. Zhu YL, Pilon-Smits EA, Tarun AS, Weber SU, Jouanin L, Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121:1169–1178CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Microbial Biotechnology and Cell BiologyUniversity of DebrecenDebrecenHungary

Personalised recommendations