Microbially Supported Phytoremediation of Heavy Metal Contaminated Soils: Strategies and Applications

Advances in Biochemical Engineering/Biotechnology

Volumn 141, Issue , 2014, Pages 211-235

  Phieler, René ^a   Voit, Annekatrin ^a   Kothe, Erika ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Microbially assisted remediation; Phytomining; Phytoremediation

Indexed keywords

HEAVY METAL; SOIL; SOIL POLLUTANT;

BACTERIA; BIOREMEDIATION; CHEMISTRY; FUNGUS; METABOLISM; MICROBIAL CONSORTIUM; MICROBIOLOGY; MYCORRHIZA; PH; PHYSIOLOGY; PLANT; SOIL; SOIL POLLUTANT; SYMBIOSIS;

BACTERIA; BIODEGRADATION, ENVIRONMENTAL; FUNGI; HYDROGEN-ION CONCENTRATION; METALS, HEAVY; MICROBIAL CONSORTIA; MYCORRHIZAE; PLANTS; SOIL; SOIL POLLUTANTS; SYMBIOSIS;

EID: 84906854216     PISSN: 07246145     EISSN: None     Source Type: Book Series    
DOI: 10.1007/10_2013_200     Document Type: Article

References (138)

1. McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232:207-214
2. Memon AR, Schröder P (2009) Implications of metal accumulation mechanisms to phytoremediation. Env Sci Pollut Res 16:162-175
3. Haferburg G, Kothe E (2010) Metallomics: lessons for metalliferous soil remediation. Appl Microbiol Biotechnol 87:1271-1280
4. Hassan Z, Aarts MGM (2011) Opportunities and feasibilities for biotechnological improvement of Zn, Cd or Ni tolerance and accumulation in plants. Env Exp Bot 72:53-63
5. Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal- contaminated land. A review. Env Chem Lett 8:1-17
6. 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 18:355-364
7. Sheoran V, Sheoran AS, Poonia P (2011) Role of hyperaccumulators in phytoextraction of metals from contaminated mining sites: A review. Crit Rev Env Sci Technol 41:168-214
8. Gardea-Torresdey JL, Peralta-Videa JR, de la Rosa G, Parsons JG (2005) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Coord Chem Rev 249:1797-1810
9. Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730-750
10. Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotox Env Safety 45:198-207
11. Schmidt A, Haferburg G, Sineriz M, Merten D, Büchel G, Kothe E (2005) Heavy metal resistance mechanisms in actinobacteria for survival in AMD contaminated soils. Chem Erde Geochem 65:131-144
12. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? and what makes them so interesting? Plant Sci 180:169-181
13. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Ann Rev Plant Physiol Plant Mol Biol 49:643-668
14. Kordel W, Dassenakis M, Lintelmann J, Padberg S (1997) The importance of natural organic material for environmental processes in waters and soils. Pure Appl Chem 69:1571-1600
15. Yanez L, Ortiz D, Calderon J, Batres L, Carrizales L, Mejia J, Martinez L, Garcia-Nieto E, Diaz-Barriga F (2002) Overview of human health and chemical mixtures: problems facing developing countries. Env Health Perspect 110:901-909
16. Salt DE, Blaylock M, Kumar N, Dushenkov V, Ensley BD, Chet I, Raskin I (1995) Phytoremediation-a novel strategy for the removal of toxic metals from the environment using plants. Bio-Technol 13:468-474
17. Mulligan CN, Yong RN, Gibbs BF (2001) Remediation technologies for metal- contaminated soils and groundwater: an evaluation. Eng Geol 60:193-207
18. Arthur EL, Rice PJ, Anderson TA, Baladi SM, Henderson KLD, Coats JR (2005) Phytoremediation-an overview. Critical Rev Plant Sci 24:109-122
19. Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper-accumulation metals in plants. Water Air Soil Pollut 184:105-126
20. Mulligan CN, Yong RN, Gibbs BF (1999) On the use of biosurfactants for the removal of heavy metals from oil-contaminated soil. Env Progress 18:50-54
21. Cunningham SD, Berti WR, Huang JW (1995) Phytoremediation of contaminated soils. Trends Biotechnol 13:393-397
22. Cunningham SD, Shann JR, Crowley DE, Anderson TA (1997) Phytoremediation of contaminated water and soil. Am Chem Soc 664:2-17
23. Raskin I, Salt D, Krämer U, Schulman R (1998) Phytoremediation: green and clean. Acta Horticult (ISHS) 457:329-332
24. Raskin I, Kumar PBAN, Dushenkov S, Salt DE (1994) Bioconcentration of heavy metals by plants. Curr Opin Biotechnol 5:285-290
25. Cunningham SD, Anderson TA, Schwab AP, Hsu FC (1996) Phytoremediation of soils contaminated with organic pollutants. Adv Agron 56:55-114
26. Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJM (1997) Phytoremediation of soil metals. Curr Opin Biotechnol 8:279-284
27. Dushenkov S, Kapulnik Y, Blaylock M, Sorochisky B, Raskin I, Ensley B (1997) Phytoremediation: a novel approach to an old problem. Studies Env Sci 66:563-572
28. Dushenkov S, Vasudev D, Kapulnik Y, Gleba D, Fleisher D, Ting KC, Ensley B (1997) Removal of uranium from water using terrestrial plants. Env Sci Technol 31:3468-3474
29. Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Env Sci Technol 29:1232-1238
30. Burken JG, Schnoor JL (1997) Uptake and metabolism of atrazine by poplar trees. Env Sci Technol 31:1399-1406
31. Baker AJM, McGrath SP, Sidoli CMD, Reeves RD (1994) The possibility of in situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants. Resour Conserv Recycl 11:41-49
32. Vangronsveld J, Colpaert JV, van Tichelen KK (1996) Reclamation of a bare industrial area contaminated by non-ferrous metals: physico-chemical and biological evaluation of the durability of soil treatment and revegetation. Env Pollut 94:131-140
33. Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees-a review. Env Int 29:529-540
34. Anderson CWN, Brooks RR, Chiarucci A, LaCoste CJ, Leblanc M, Robinson BH, Simcock R, Stewart RB (1999) Phytomining for nickel, thallium and gold. J Geochem Expl 67:407-415
35. Boyd V (1996) Pint-sized plants pack a punch in fight against heavy metals. Env Prot 7:38-39
36. Pilon-Smits E (2005) Phytoremediation. Ann Rev Plant Biol 56:15-39
37. Huang JWW, Chen JJ, Berti WR, Cunningham SD (1997) Phytoremediation of lead- contaminated soils: role of synthetic chelates in lead phytoextraction. Env Sci Technol 31:800-805
38. Ernst WHO (2005) Phytoextraction of mine wastes-options and impossibilities. Chem Erde Geochem 65:29-42
39. Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresource Technol 77:229-236
40. Boyd RS, Jaffre T, Odom JW (1999) Variation in nickel content in the nickel- hyperaccumulating shrub Psychotria douarrei (Rubiaceae) from New Caledonia. Biotropica 31:403-410
41. van Nevel L, Mertens J, Oorts K, Verheyen K (2007) Phytoextraction of metals from soils: how far from practice? Env Pollut 150:34-40
42. Mendez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments-an emerging remediation technology. Env Health Perspect 116:278-283
43. Kucharski R, Sas-Nowosielska A, Malkowski E, Japenga J, Kuperberg JM, Pogrzeba M, Krzyzak J (2005) The use of indigenous plant species and calcium phosphate for the stabilization of highly metal-polluted sites in southern Poland. Plant Soil 273:291-305
44. Yoon J, Cao XD, Zhou QX, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Env 368:456-464
45. Geebelen W, Adriano DC, van der Lelie D, Mench M, Carleer R, Clijsters H, Vangronsveld J (2003) Selected bioavailability assays to test the efficacy of amendment-induced immobilization of lead in soils. Plant Soil 249:217-228
46. Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, van der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Env Sci Pollut Res 16:765-794
47. Pichtel JR, Dick WA, Sutton P (1994) Comparison of amendments and management practices for long-term reclamation of abandoned mine lands. J Env Qual 23:766-772
48. Dushenkov S, Kumar PBAN, Motto H, Raskin I (1995) Rhizofiltration: The use of plants to remove heavy metals from aqueous streams. Env Sci Technol 29:1239-1245
49. Macaskie LE (1991) The application of biotechnology to the treatment of wastes produced from the nuclear fuel cycle: Biodegradation and bioaccumulation as a means of treating radionuclide-containing streams. Crit Rev Biotechnol 11:41-112
50. Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139-153
51. Kaschl A, Romheld V, Chen Y (2002) Cadmium binding by fractions of dissolved organic matter and humic substances from municipal solid waste compost. J Env Qual 31:1885-1892
52. Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8:221-226
53. Welch RM, Norvell WA, Schäfer SC, Shaff JE, Kochian LV (1993) Induction of iron(III) and copper(II) reduction in pea (Pisum sativum L.) roots by Fe and Cu status-does the root-cell plasmalemma Fe(III)-chelate reductase perform a general role in regulating cation uptake. Planta 190:555-561
54. Lagier T, Feuillade G, Matejka G (2000) Interactions between copper and organic macromolecules: determination of conditional complexation constants. Agronomie 20:537-546
55. Halim M, Conte P, Piccolo A (2003) Potential availability of heavy metals to phytoextraction from contaminated soils induced by exogenous humic substances. Chemosphere 52:265-275
56. Zhou J-M, Dang Z, Chen N-C, Xu S-G, Xie Z-Y (2007) Enhanced phytoextraction of heavy metal contaminated soil by chelating agents and auxin indole-3-acetic acid. Huan Jing Ke Xue 28:2085-2088
57. Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128:1120-1128
58. Lasat MM (2002) Phytoextraction of toxic metals: a review of biological mechanisms. J Env Qual 31:109-120
59. Kagi JH, Kojima Y (1979) Nomenclature of metallothionein: a proposal. Experientia Suppl 34:141-142
60. Lane B, Kajioka R, Kennedy T (1987) The wheat-germ Ec protein is a zinc-containing metallothionein. Biochem Cell Biol-Biochim Biol Cellulaire 65:1001-1005
61. Murphy A, Zhou JM, Goldsbrough PB, Taiz L (1997) Purification and immunological identification of metallothioneins 1 and 2 from Arabidopsis thaliana. Plant Physiol 113:1293-1301
62. Schmidt A, Hagen M, Schütze E, Schmidt A, Kothe E (2010) In silico prediction of potential metallothioneins and metallohistins in actinobacteria. J Basic Microbiol 50:562-569
63. Rauser WE (1995) Phytochelatins and related peptides (structure, biosynthesis, and function). Plant Physiol 109:1141-1149
64. Grill E, Löffler S, Winnacker E-L, Zenk MH (1989) Phytochelatins, the heavy-metal- binding peptides of plants, are synthesized from glutathione by a specific c-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase). Proc Nat Acad Sci U S A 86:6838-6842
65. Thumann J, Grill E, Winnacker E-L, Zenk MH (1991) Reactivation of metal-requiring apoenzymes by phytochelatin-metal complexes. FEBS Lett 284:66-69
66. Yang X-E, Jin X-F, Feng Y, Islam E (2005) Molecular mechanisms and genetic basis of heavy metal tolerance/hyperaccumulation in plants. J Integr Plant Biol 47:1025-1035
67. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395-412
68. 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 107:1687-1696
69. Ma Y, Prasad MN, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248-258
70. Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Gen Mol Biol 35:1044-1051
71. Kloepper JW, Schroth MN (1979) Plant-growth promoting rhizobacteria-evidence that the mode of action involves root microflora interactions. Phytopathology 69:1020-1024
72. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847-859
73. Neilands JB (1984) Methodology of siderophores. Struct Bonding 58:1-24
74. Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant-growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885-886
75. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844-2854
76. Dimkpa C, Svatos A, Merten D, Büchel G, Kothe E (2008) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54:163-172
77. Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19-25
78. Dimkpa C, Weinand T, Asch F (2009) Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Env 32:1682-1694
79. Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318-333
80. Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153-160
81. Misaghi IJ, Donndelinger CR (1990) Endophytic bacteria in symptom-free cotton plants. Phytopathology 80:808-811
82. Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, van der Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583-606
83. Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water- soluble, volatile, organic pollutants. Nature Biotechnol 22:583-588
84. Germaine KJ, Keogh E, Ryan D, Dowling DN (2009) Bacterial endophyte-mediated naphthalene phytoprotection and phytoremediation. FEMS Microbiol Lett 296:226-234
85. Germaine KJ, Liu X, Cabellos GG, Hogan JP, Ryan D, Dowling DN (2006) Bacterial endophyte- enhanced phytoremediation of the organochlorine herbicide 2,4-dichlorophenoxyacetic acid. FEMS Microbiol Ecol 57:302-310
86. Weyens N, Croes S, Dupae J, Newman L, van der Lelie D, Carleer R, Vangronsveld J (2010) Endophytic bacteria improve phytoremediation of Ni and TCE co-contamination. Env Pollut 158:2422-2427
87. Selosse MA, Baudoin E, Vandenkoornhuyse P (2004) Symbiotic microorganisms, a key for ecological success and protection of plants. Crit Rev Biol 327:639-648
88. Kothe E, Dudeja SS (2011) Editorial. J Basic Microbiol 51:4
89. Dudeja SS, Giri R, Saini R, Suneja-Madan P, Kothe E (2012) Interaction of endophytic microbes with legumes. J Basic Microbiol 52:248-260
90. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Ann Rev Microbiol 59:19-42
91. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego
92. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Comm 1:48
93. Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Div 33:1-45
94. Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197-207
95. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299-363
96. Wilkins DA (1991) The influence of sheathing (ecto-) mycorrhizas of trees on the uptake and toxicity of metals. Agricult Ecosyst Env 35:245-260
97. Turnau K, Kottke I, Dexheimer J, Botton B (1994) Element distribution in mycelium of Pisolithus arrhizus treated with cadmium dust. Annals Bot 74:137-142
98. Bojarczuk K, Kieliszewska-Rokicka B (2010) Effect of ectomycorrhiza on Cu and Pb accumulation in leaves and roots of silver birch (Betula pendula Roth.) seedlings grown in metal-contaminated soil. Water Air Soil Pollut 207:227-240
99. Hrynkiewicz K, Dabrowska G, Baum C, Niedojadlo K, Leinweber P (2012) Interactive and single effects of ectomycorrhiza formation and Bacillus cereus on metallothionein MT1 expression and phytoextraction of Cd and Zn by willows. Water Air Soil Pollut 223:957-968
100. Bonfante P (2010) Plant-fungal interactions in mycorrhizas., Encyclopedia of Life SciencesWiley, London
101. Narula N, Reinicke M, Haferburg G, Kothe E, Behl RK (2012) Plant-microbe interaction in heavy metal-contaminated soils. In: Kothe E, Varma A (eds) Bio-geo interactions in heavy metal-contaminated soils. Springer, Heidelberg, pp 143-162
102. Ebenå G, Kothe E (2006) Bioleaching and microbial mineral degradation. In: Varma A (ed) Microbes: health and environment, vol 3. IK International Publishing, New Delhi, pp 389-405
103. Haferburg G, Kothe E (2012) Biogeosciences in heavy metal-contaminated soils. In: Kothe E, Varma A (eds) Bio-geo interactions in heavy metal-contaminated soils. Springer, Heidelberg, pp 17-34
104. Schindler F, Gube M, Kothe E (2012) Bioremediation and heavy metal uptake: microbial appraoches at field scale. In: Koth E, Varma A (eds) Bio-geo interactions in heavy metal- contaminated soils. Springer, Heidelberg, pp 365-384
105. Merten D, Geletneky J, Bergmann H, Haferburg G, Kothe E, Büchel G (2005) Rare earth element patterns: a tool for remediation of acid mine drainage. Chem Erde Geochem 65S1:97-114
106. Schmidt A, Haferburg G, Schmidt A, Lischke U, Merten D, Gherghel F, Büchel G, Kothe E (2009) Heavy metal resistance to the extreme: Streptomyces strains from a former uranium mining area. Chem Erde Geochem 69:35-44
107. Haferburg G, Klöß G, Schmitz W, Kothe E (2008) Ni-struvite-a new biomineral formed by a nickel resistant Streptomyces acidiscabies. Chemosphere 72:517-523
108. Kothe E, Dimkpa CO, Haferburg G, Schmidt A, Schmidt A, Schütze E (2010) Streptomycete heavy metal resistance: extracellular and intracellular mechanisms. In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Heidelberg, pp 225-236
109. Pitman M (1972) Uptake and transport of ions in barley seedlings II. Evidence for two active stages in transport to the shoot. Aus J Biol Sci 25:243-258
110. Boer AH, Prins HBA, Zanstra PE (1983) Bi-phasic composition of trans-root electrical potential in roots of Plantago species: involvement of spatially separated electrogenic pumps. Planta 157:259-266
111. Stephan UW, Schmidke I, Stephan VW, Scholz G (1996) The nicotianamine molecule is made-to-measure for complexation of metal micronutrients in plants. Biometals 9:84-90
112. Vögeli-Lange R, Wagner GJ (1990) Subcellular localization of cadmium and cadmium- binding peptides in tobacco leaves: implication of a transport function for cadmium-binding peptides. Plant Physiol 92:1086-1093
113. Kupper H, Zhao FJ, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305-311
114. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1:81-126
115. Prasad MNV (2005) Nickelophilous plants and their significance in phytotechnologies. Braz J Plant Physiol 17:113-128
116. Boyd RS, Shaw JJ, Martens SN (1994) Nickel hyperaccumulation defends Streptanthus polygaloides (Brassicaceae) against pathogens. Am J Bot 81:294-300
117. Boyd RS, Martens SN (1994) Nickel hyperaccumulated by Thlaspi montanum var. montanum is acutely toxic to an insect herbivore. Oikos 70:21-25
118. Chaney RL (1983) Plant uptake of inorganic waste. In: Parr JE, Marsh PB, Kla JM (eds) Land treatment of hazardous waste. Noyes Data Corp, Park Ridge, pp 50-76
119. McGrath SP, Sidoli CMD, Baker AJM, Reeves RD (1993) The potential for the use of metal-accumulating plants for the in situ decontamination of metal-polluted soils. In: Eijsackers HJP, Hamers T (eds) Integrated soil and sediment research: a basis for proper prediction. Kluwer, Dordrecht, The Netherlands, pp 673-676
120. Nicks L, Chambers MF (1998) A pioneering study of the potential of phytomining for nickel. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford, pp 312-325
121. Nicks L, Chambers MF (1995) Farming for metals. Mining Environ Meeting 199:15-18
122. Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Expl 60:115-126
123. Brooks RR, Robinson BH, Howes AW, Chiarucci A (2001) An evaluation of Berkheya coddii Roessler and Alyssum bertolonii Desv. for phytoremediation and phytomining of nickel. S Afr J Sci 97:558-560
124. Brooks RR, Robinson BH (1998) The potential use of hyperaccumulators and other plants for phytomining. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals: their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining. CAB International, Wallingford, pp 327-356
125. Robinson BH, Banuelos G, Conesa HM, Evangelou MWH, Schulin R (2009) The phytomanagement of trace elements in soil. Critical Rev Plant Sci 28:240-266
126. Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23:6-8
127. Mastretta C, Barac T, Vangronsveld J, Newman L, Taghavi S, van der Lelie D (2006) Endophytic bacteria and their potential application to improve the phytoremediation of contaminated environments. Biotechnol Genet Eng Rev 23:175-207
128. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1-9
129. Gatzweiler R, Jakubick AT, Meyer J, Paul M, Schreyer J (2003) Flooding of the WISMUT mines - learning by doing or applying a comprehensive systematic approach? In: Merkel B, Planer-Friedrich B, Wolkersdorfer C (eds) Uranium in the aquatic environment. Springer, Heildelberg, pp 745-754
130. Grawunder A, Lonschinski M, Merten D, Büchel G (2009) Distribution and bonding of residual contamination in glacial sediments at the former uranium mining leaching heap of Gessen/Thuringia, Germany. Chem Erde - Geochem 69S2:5-19
131. Lonschinski M, Knöller K, Merten D, Büchel G (2011) Flow dynamics of groundwater and soil water in the former heap Gessenhalde at the uranium mining area of Ronneburg: a stable isotope approach. Hydrol Process 25:861-872
132. Senitz S, Gaupp R, Büchel G (2009) Hochaufgelöste dreidimensionale Rekonstruktion eines quartären Talaquifers in einem Teilbereich des Gessentals bei Ronneburg (ehemaliges ostthüringisches Uranerzbergbaurevier) durch die Kombination von Geländedaten und geostatistischer Schätzung. Zeitschr dtsch Ges Geowiss 160:367-389
133. Kothe E, Bergmann H, Büchel G (2005) Molecular mechanisms in bio-geo-interactions: from a case study to general mechanisms. Chem Erde Geochem 65S1:7-27
134. Willscher S, Mirgorodsky D, Jablonski L, Ollivier D, Merten D, Büchel G, Wittig J, Werner P (2013) Field scale phytoremediation experiments on a heavy metal and uranium contaminated site, and further utilization of the plant residues. Hydrometallurgy F:46-53
135. Büchel G, Bergmann H, Ebenå G, Kothe E (2005) Geomicrobiology in remediation of mine waste. Chem Erde 65S1:1-5
136. Mirgorodsky D, Ollivier D, Merten D, Bergmann H, Büchel G, Willscher S, Wittig J, Jablonski L, Werner P (2010) Radiation protection of radioactively contaminated large areas by phytoremediation and subsequent utilization of the contaminated plant residues. J Nucl Power 55:774-778
137. Demchik MC, Sharpe WE (2001) Forest floor plant response to lime and fertilizer before and after partial cutting of a northern red oak stand on an extremely acidic soil in Pennsylvania, USA. Forest Evol Manag 144:239-244
138. Reinicke M, Schindler G, Roth M, Kothe E (2013) Multi-metal bioremediation by microbial assisted phytoremediation. In: Actinobacteria. Application in bioremediation and production of industrial enzymes (Amorosos MJ, Benimeli CS, Cuozzo SA, Eds.). CRC, Boca Raton, USA, pp 87-105.