Abstract
Pollution of the biosphere by heavy metals (HM) is a global threat that has accelerated dramatically since the beginning of industrial revolution. HMs can accumulate in soil and, in turn, adversely affect the microbial population density and physicochemical properties of soils, leading to the loss of soil fertility and yields of crops. The HMs generally cannot be biologically degraded to more or less toxic products and, hence, persist in the environment. Conventional methods used for metal detoxification produce large quantities of toxic products and are not cost-effective. The use of microorganisms (bioremediation) and plants (phytoremediation) to remediate polluted environments has provided an alternative to conventional methods for the cleaning-up of soils contaminated by metals. Phytoremediation mostly involves the use of metal-hyperaccumulating plants to remove, transform, or stabilize the contaminants, but this technique is time consuming. In other words, plants with exceptionally high metal-accumulating capacity often have a slow growth rate and produce limited amounts of biomass when the concentration of metal in the contaminated soil is very high and toxic. Microorganisms also play important roles in the environmental fate of toxic metals and metalloids with a multiplicity of physicochemical and biological mechanisms affecting transformations between soluble and insoluble phases. Furthermore, by establishing effective relationships with plants, microorganisms are able to induce the chance of success of phytoremediation. Fungi, particularly arbuscular mycorrhizal fungi (AMF), associated with hyperaccumulating or non-hyperaccumulating plants have repeatedly been demonstrated to alleviate HM stress of plants, although there is a need to completely understand the ecological complexities of their interactions with the host plant and soil system and their better exploitation as consortia in remediation strategies employed for contaminated soils. This chapter provides an overview on the developments in the role of fungi particularly AMF in phytorestoration of HM-contaminated soils.
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References
Alkorta I, Aizpurua A, Riga P, Albizu I, Amezaga I, Garbisu C (2003) Soil enzyme activities as biological indicators of soil health. Rev Environ Health 18:65–73
Alloway BJ, Jackson AP (1991) The behavior of heavy metals in sewage sludge amended soils. Sci Total Environ 100:151–176
Alonso J, Garcia AM, Pérez-López M, Melgar MJ (2003) The concentrations and bioconcentration factors of copper and zinc in edible mushrooms. Arch Environ Contam Toxicol 44:180–188
Anderson TA, Coats JR (1994) Bioremediation through rhizosphere technology, vol 563, ACS symposium series. American Chemical Society, Washington, DC, p 249
Aoyama M, Itaya S, Otowa M (1993) Effects of copper on the decomposition of plant residues, microbial biomass and beta-glucosidase activity in soils. Soil Sci Plant Nutr 39:557–566
Arisi ACM, Noctor G, Foyer CH, Jouanin L (2003) Modification of thiol contents in poplars (Populus tremula × P. alba) overexpressing enzymes involved in glutathione synthesis. Planta 203:362–372
Arnold PT, Kaputska LA (1987) VA mycorrhizal colonization and spore populations in abandoned agricultural field after five years of sludge additions. Ohio J Sci 87:112–114
Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362
Assunçao AGL, Da Costa MP, De Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24:217–226
Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations: a review. Water Air Soil Pollut 47:335–379
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
Balsalobre C, Calonge J, Jiménez E, Lafuente R, Mouriño M, Muño MT, Riquelme M, Mas-Castella J (1993) Using the metabolic capacity of Rhodobacter sphaeroides to assess heavy metal toxicity. Environ Toxicol Water Qual 8:437–450
Barceló J, Poschenrieder C (2003) Phytoremediation: principles and perspectives. Contrib Sci 2: 333–344
Bardgett RD, Speir TW, Ross DJ, Yeats GW, Kettles HA (1994) Impact of pasture contamination by copper, chromium, and arsenic timber preservative on soil microbial properties and nematodes. Biol Fertil Soils 18:71–79
Begonia MT, Begonia GB, Miller G, Gilliard D, Young C (2004) Phosphatase activity and populations of microorganisms from cadmium and lead contaminated soils. Bull Environ Contam Toxicol 73:1025–1032
Bending GD, Turner MK, Rayns F, Marx MC, Wood M (2004) Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes. Soil Biol Biochem 36:1785–1792
Berdicevsky I, Duek L, Merzbach D, Yannai S (1993) Susceptibility of different yeast species to environmental toxic metals. Environ Pollut 80:41–44
Bogomolov DM, Chen SK (1996) An ecosystem approach to soil toxicity testing—A study of copper contamination in laboratory soil microscosms. Appl Soil Ecol 4:95–105
Bohn KS and Liberta AE (1982) In: Graves DH (ed) Symposium on surface mining hydrology, sedimentology and reclamation. University of Kentucky, Lexington
Boyle M, Paul EA (1988) Vesicular-arbuscular mycorrhizal associations with barley on sewage-amended plots. Soil Biol Biochem 20:945–948
Brenner V, Arensdorf JJ, Foght DD (1994) Genetic construction of PCB degraders. Biodegradation 5:359–377
Brookes PC (1995) The use of microbial parameters in monitoring soil pollution by heavy metals. Biol Fertil Soils 19:269–279
Brooks RR (1998) Geobotany and hyperaccumulators. In: Brook RR (ed) Plants that hyperaccumulate heavy metals. CAB, Walingford, pp 55–94
Brown PE, Minges GA (1916) The effect of some manganese salts on ammonification and nitrification. Soil Sci 1:67–85
Chen B, Christie P, Li X (2001) A modified glass bead compartment cultivation system for studies on nutrient and trace metal uptake by arbuscular mycorrhiza. Chemosphere 42:185–192
Chen BD, Li XL, Tao HQ, Christie P, Wong MH (2003) The role of arbuscular mycorrhiza in zinc uptake by red clover growing in a calcareous soil spiked with various quantities of zinc. Chemosphere 50:839–846
Christie P, Beattie JAM (1989) Grassland soil microbial biomass and accumulation of potentially toxic metals from long term slurry application. J Appl Ecol 26:597–612
Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216
Compant S, Clément B, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Crutzen PJ (1970) The influence of nitrogen oxides on the atmospheric ozone content. Q J R Meteorol Soc 96:320–325
Cunningham SD, Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol 110:715–719
Cunningham SD, Shann JR, Crowley DE, Anderson TA (1997) Phytoremediation of contaminated water and soil. In: Kruger EL, Anderson TA, Coats JR (eds.) Phytoremediation of soil and water contaminants. ACS symposium series 664. American Chemical Society, Washington, DC, pp. 2–19
Dahlin S, Witter E, Mårtensson AM, Turner A, Bååth E (1997) Where’s the limit? Changes in the microbiological properties of agricultural soils at low levels of metal contamination. Soil Biol Biochem 29:1405–1415
Danika L, Duc L, Terry N (2005) Phytoremediation of toxic trace elements in soil and water. J Ind Microbiol Biotechnol 32:514–520
Dedourge O, Vong PC, Lasserre-Joulin F, Benizri E, Guckert A (2004) Effect of glucose and rhizodeposits (with or without cysteine-S) on immobilized-35S, microbial biomass-35S and arylsulphatase activity in a calcareous and an acid brown soil. Eur J Soil Sci 55:649–656
Del Val C, Barea JM, Azcon-Aguilar C (1999) Assessing the tolerance to heavy metals of arbuscular mycorrhizal fungi isolated from sewage sludge-contaminated soils. Appl Soil Ecol 11:261–269
Delorme TA, Gagliardi JV, Angle JS, Chaney RL (2001) Influence of the zinc hyperaccumulator Thlaspi caerulescens J. & C. Presl. and the nonmetal accumulator Trifolium pratense L. on soil microbial populations. Can J Microbiol 47:773–776
Diaz G, Honrubia M (1994) A mycorrhizal survey of plants growing on mine wastes in southeast Spain. Arid Soil Res Rehabil 8:59–68
Diaz G, Azcon-Aguilar C, Honrubia M (1996) Influence of arbuscular mycorrhizae on heavy metal (Zn and Pb) uptake and growth of Lygeum spartum and Anthillis cystisoides. Plant Soil 180: 1201–1205
Dickinson RE, Cicerone RJ (1986) Future global warming from atmospheric trace gases. Nature 319:109–115
Dmitri S, Begonia FT (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 5:450–456
Dodd JC, Thompson BD (1994) The screening and selection of inoculant arbuscular mycorrhizal and ectomycorrhizal fungi. Plant Soil 159:149–158
Doelman P, Haanstra L (1984) Short-term and long-term effects of cadmium, chromium, copper, nickel, lead and zinc on soil microbial respiration in relation to abiotic soil factors. Plant Soil 79:317–327
Dueck TA, Visser P, Ernst WHO, Schat H (1986) Vesicular-arbuscular mycorrhizae decrease zinc toxicity to grasses growing in zinc polluted soils. Soil Biol Biochem 18:331–333
Elekes CC, Busuoic G, Ionita G (2010) The mycoremediation of metals polluted soils using wild growing species of mushrooms. Latest trends on engineering education. Not Bot Horti Agrobot Cluj Napoca 38:147–151
Filser J, Fromm H, Nagel RF, Winter K (1995) Effects of previous intensive agricultural management on microorganisms and the biodiversity of soil fauna. Plant Soil 170:123–129
Fritze H, Vanhala P, Pietikäinen J, Mälkönen E (1996) Vitality fertilization of Scots pine stands growing along a gradient of heavy metal pollution: short-term effects on microbial biomass and respiration rate of the humus layer. Fresenius J Anal Chem 354:750–755
Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass and activity of microbial communities from two soil types experimentally exposed to different metals. Appl Environ Microbiol 59:3605–3617
Frostegård Å, Tunlid A, Bååth E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28: 55–63
Fulladosa E, Murat JC, Martínez M, Villaescusa I (2005a) Patterns of metals and arsenic poisoning in Vibrio fischeri. Chemosphere 60:43–48
Fulladosa E, Murat JC, Villaescusa I (2005b) Study on the toxicity of binary equitoxic mixtures of metals using the luminescent bacteria Vibrio fischeri as a biological target. Chemosphere 58(5):551–557
Gadd GM (2001) Fungi in bioremediation. Cambridge University Press, Cambridge
Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643
Gadd GM, White C (1989) Heavy metal and radionuclide accumulation and toxicity in fungi and yeasts. In: Poole RK, Gadd GM (eds) Metal-microbe interactions. Special publication of the Society for General Microbiology, vol 26. IRL/Oxford University Press, New York, pp 19–38
Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sun-flower leaves: evidence for involvement of oxidative stress. Plant Sci 121:151–159
Gang WU, Kang H, Xiaoyang Z, Hongbo S, Liye C, Chengjiang R (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 174:1–8
Garbisu C, Hernandez-Allica J, Barrutia O, Alkorta I, Becerril JM (2002) Phytoremediation: a technology using green plants to remove contaminants from polluted areas. Rev Environ Health 17:75–90
Gasper GM, Mathe P, Szabo L, Orgovanyl B, Uzinger N, Anton A (2005) After-effect of heavy metal pollution in brown forest soils. Proceedings of the 8th Hungarian Congress on Plant Physiology and the 6th Hungarian Conference on Photosynthesis. Acta Biologica Szegediensis 49:71–72
Gast CH, Jansen E, Bierling J, Haanstra L (1998) Heavy metals in mushrooms and their relationship with soil characteristics. Chemosphere 17:789–799
Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci 86:528–534
Geiger G, Federer P, Sticher H (1993) Reclamation of heavy metal-contaminated soils: field studies and germination experiments. J Environ Qual 22:201–207
Giasson P, Jaouich A, Gagné S, Massicotte L, Cayer P, Moutoglis P (2006) Enhanced phytoremediation: a study of mycorrhizoremediation of heavy metal contaminated soil. Remediation 17:97–110
Gibson DT, Parales RE (2000) Aromatic hydrocarbons dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243
Gildon A, Tinker PB (1981) A heavy metal-tolerant strain of mycorrhizal fungus. Trans Br Mycol Soc 77:648–649
Gildon A, Tinker PB (1983) Interactions of vesicular-arbuscular mycorrhizal infection and heavy metals in plants. The effects of heavy metals on the development of vesicular-arbuscular mycorrhizas. New Phytol 95:247–261
Giller KE, Beare MH, Lavelle P, Izac MN, Swift MJ (1997) Agricultural intensification, soil biodiversity and ecosystem function. Appl Soil Ecol 6:3–16
Glazer AN, Nikaido H (2007) Microbial biotechnology: fundamentals of applied microbiology, 2nd edn. Cambridge University press, Cambridge, pp 510–528
Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393
Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122
Gonzalez-Chavez C, Harris PJ, Dodd J, Meharg AA (2002) Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytol 155:163–171
Gonzalez-Chavez MC, Vangronsveld J, Colpaert J, Leyval C (2006) Arbuscular mycorrhizal fungi and heavy metals: tolerance mechanisms and potential use in bioremediation. In: Prasad MNV, Sajwan KS, Naidu R (eds) Trace elements in the environment. Biogeochemistry, biotechnology, and bioremediation. CRC, Boca Raton, FL, pp 211–234
Gremion F, Chatzinotas A, Kaufmann K, Von Sigler W, Harms H (2004) Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS Microbiol Ecol 48:273–283
Gupta SK (1992) Mobilizable metal in anthropogenic contaminated soils and its ecological significance. In: Vernet JP (ed) Impact of heavy metals on the environment. Elsevier, Amsterdam, pp 299–310
Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53: 1–11
Hammer D, Kayser A, Keller C (2003) Phytoextraction of Cd and Zn with Salix viminalis in field trials. Soil Use Manag 19:187–192
Harris PJ (1994) Consequences of the spatial distribution of microbial communities in soil. In: Ritz K, Dighton J, Giller KE (eds) Beyond the biomass. Compositional and functional analysis of soil microbial communities. Wiley, Chichester, pp 239–246
Hartley-Whitaker J, Ainsworth G, Vooijs R, Ten Bookum W, Schat H, Meharg AA (2001) Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus. Plant Physiol 126:299–306
Haselwandter K, Leyval C, Sanders FE (1994) Impact of arbuscular mycorrhizal fungi on plant uptake of heavy metals and radionuclides from soil. In: Gianinazzi S, SchuÈepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. BirkhaÈuser, Basel, pp 179–189
Hattori H (1996) Decomposition of organic matter with previous cadmium adsorption in soils. Soil Sci Plant Nutr 42:745–752
Hernandez-Allica J, Becerril JM, Zarate O, Garbisu C (2006) Assessment of the efficiency of a metal phytoextraction process with biological indicators of soil health. Plant Soil 281:147–158
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemisrty 68:139–146
Hinojosa MB, Carreira J, García-Ruíza R, Dick RP (2004) Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils. Soil Biol Biochem 36:1559–1568
Holtan-Hartwig L, Bechmann M, Høyås TR, Linjordet R, Bakken LR (2002) Heavy metals tolerance of soil denitrifying communities: N2O dynamics. Soil Biol Biochem 34:1181–1190
Homer FA, Reeves RD, Brooks RR (1997) The possible involvement of aminoacids in nickel chelation in some nickel-accumulating plants. Curr Top Phytochem 14:31–33
Howden R, Anderson CR, Goldsbrough PB, Cobbett CS (1995) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol 107:1067–1073
Hüttermann A, Arduini I, Godbold DL (1999) Metal pollution and forest decline. In: Prasad NMV, Hagemeyer J (eds) Heavy metal stress in plants: from molecules to ecosystems. Springer, Berlin, pp 253–272
Illmer P, Schinner F (1991) Effects of lime and nutrient salts on the microbiological activities of forest soils. Biol Fertil Soils 11:261–266
Insam H, Domsch KH (1988) Relationship between soil organic carbon and microbial biomass on chronosequences of reclamation sites. Microb Ecol 15:177–188
Jentschke G, Godbold DL (2000) Metal toxicity and ectomycorrhizas. Physiol Plant 109:107–116
Kabata-Pendias A (2001) Trace elements in soils and plants, 3rd edn. CRC, Boca Raton, FL
Kabata-Pendias A, Mukherjee AB (2007) Trace elements from soil to human. Springer, Heidelberg, 550 pp
Kaldorf M, Kuhn A, Schroder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728
Kandeler E, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Biol Fertil Soils 23:299–306
Kandeler E, Tscherko D, Bruce KD, Stemmer M, Hobbs PJ, Bardgett RD, Amelung W (2000) Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biol Fertil Soils 32:390–400
Kayser A, Wenger K, Keller A, Attinger W, Felix HR, Gupta SK, Schulin R (2000) Enhancement of phytoextraction of Zn, Cd, and Cu from calcareous soil: the use of NTA and sulfur amendments. Environ Sci Technol 34:1778–1783
Kazumasa H, Naoki T, Kazuhisa M (2005) Biosynthetic regulation of phytochelatins, heavy metal-binding peptides. J Biosci Bioeng 100:593–599
Keller C, McGrath SP, Dunham SJ (2002) Trace metal leaching through a soil–grassland system after sewage sludge application. J Environ Qual 31:1550–1560
Kelly JJ, Haggblom MM, Tate RL (2003) Effects of heavy metal contamination and remediation on soil microbial communities in the vicinity of a zinc smelter as indicated by analysis of microbial community phospholipids fatty acid profiles. Biol Fertil Soils 38:65–71
Keshav PS, Nand KS, Shivesh S (2010) Bioremediation: developments, current practices and perspectives. Genet Eng Biotechnol J 2010:1–20
Khade SW, Adholeya A (2007) Feasible bioremediation through arbuscular mycorrhizal fungi imparting heavy metal tolerance: a retrospective. Bioremediat J 11:33–43
Khan AG (2006) Mycorrhizoremediation—an enhanced form of phytoremediation. J Zhejiang Univ Sci B 7:503–514
Khodaverdiloo H, Homaee M (2008) Modeling of cadmium and lead phytoextraction from contaminated soil. Pol J Soil Sci 41:149–162
Knight B, McGrath SP, Chaudri AM (1997) Biomass carbon measurements and substrate utilization patterns of microbial populations from soils amended with cadmium, copper or zinc. Appl Environ Microbiol 63:39–43
Kuperman RG, Carreiro MM (1997) Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem. Soil Biol Biochem 29:179–190
Ladd JNM, Amato M, Grace PR, van Veen JA (1995) Simulation of 14C turnover through the microbial biomass in soils incubated with 14C-labelled plant residues. Soil Biol Biochem 27:777–783
Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67
Lau PCK, Lorenzo VDE (1999) Genetic engineering: the frontier of bioremediation. Environ Sci Technol 4:124A–128A
Leita L, Denobili M, Muhlbachova G, Mondini C, Marchiol L, Zerbi G (1995) Bioavailability and effects of heavy metals on soil microbial biomass survival during laboratory incubation. Biol Fertil Soils 19:103–108
Leung HM, Ye ZH, Wong MH (2006) Interactions of mycorrhizal fungi with Pteris vittata (as hyperaccumulator) in As-contaminated soils. Environ Pollut 139:1–8
Leyval C, Singh BR, Joner EJ (1995) Occurrence and infectivity of arbuscular mycorrhiza fungi in some Norwegian soils influenced by heavy metals and soil properties. Water Air Soil Pollut 84: 203–216
Leyval C, Turnau A, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7: 139–153
Lipman CB, Burgess PS (1914) The effects of copper, zinc, iron and lead salts on ammonification and nitrification in soils. Univ Calif Publ Agric Sci 1:127–139
Litz R, Lavi U (1997) Mango biotechnology (chapter 12). In: Litz R (ed) The mango. CRC, Boca Raton, FL, pp 401–424
Lombi E, Wenzel WW, Gobran GR, Adriano DC (2001) Dependency of phyto-availability of metals on indigenous and induced rhizosphere processes: a review. In: Gobran GR, Wenzel WW, Lombi E (eds) Trace elements in the rhizosphere. CRC, New York, pp 3–24
Long LK, Yao Q, Guo J, Yang RH, Huang YH, Zhu HH (2010) Molecular community analysis of arbuscular mycorrhizal fungi associated with five selected plant species from heavy metal polluted soils. Eur J Soil Biol 46:288–294
Macnair MR, Tilstone GH, Smith SE (2000) The genetics of metal tolerance and accumulation in higher plants. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soil and water. CRC, Boca Raton, FL, pp 235–250
Maliszewska W, Dec S, Wierzbicka H, Wozniakowska A (1985) The influence of various heavy metal compounds on the development and activity of soil micro-organisms. Environ Pollut A 37:195–215
Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102
Marschner B, Kalbitz K (2003) Control of bioavailability and biodegradation of dissolved organic matter in soils. Geoderma 113:211–235
Mathur NJ, Singh S, Bohra A, Vyas A (2007) Arbuscular mycorrhizal fungi: a potential tool for phytoremediation. J Plant Sci 2:127–140
McGrath SP (1994) Effects of heavy metals from sewage sludge on soil microbes in agricultural ecosystems. In: Ross SM (ed) Toxic metals in soil-plant systems. Wiley, Chichester, pp 242–274
McGrath SP, Chaudri AM, Giller KE (1995) Long term effects of metals in sewage sludge on soils, microorganisms and plants. J Ind Microbiol 14:94–104
McIntyre T (2003) Phytoremediation of heavy metals from soils. Adv Biochem Eng Biotechnol 78:97–123
Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162
Mehra RK, Mulchandani P (1995) Glutathione-mediated transfer of Cu(I) into phytochelatins. Biochem J 307:687–705
Mehra RK, Winge DR (1991) Metal ion resistance in fungi: molecular mechanisms and their regulated expression. J Cell Biochem 45:30–40
Mejare M, Bülow L (2001) Metal-binding proteins and peptides in bioremediation and phytoremediation of heavy metals. Trends Biotechnol 19:67–73
Mench MJ, Didier VL, Loffler M, Gomez A, Masson P (1994) A mimicked insitu remediation study of metalcontaminated soils with emphasis on cadmium and lead. J Environ Qual 23: 785–792
Moftah AE (2000) Physiological response of lead polluted tomato and eggplant to the antioxidant ethylene diurea. Menofia Agric Res 25:933–955
Morley GF, Sayer JA, Wilkinson SC, Gharieb MM, Gadd GM (1996) Fungal sequestration, solubilization and transformation of toxic metals. In: Frankland JC, Magan N, Gadd GM (eds) Fungi and environmental change. Cambridge University Press, Cambridge, pp 235–256
Naidu CK, Reddy TKR (1988) Effect of cadmium on microorganisms and microbe-mediated mineralization process in soil. Bull Environ Contam Toxicol 41:657–663
Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick R (eds) Enzymes in the environment. Marcel Dekker, New York, pp 1–33
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Noctor G, Arisi ACM, Jouanin L, Kuner KJ, Rennenberg H, Foyer C (1998) Glu-tathione biosynthesis metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49:623–647
Ohya H, Komai Y, Amaguchi MY (1985) Zinc effects on soil microflora and glucose metabolites in soil amended with 14C-glucose. Biol Fertil Soils 1:117–122
Ouzouni PK, Veltsistas PG, Paleologos EK, Riganakos KA (2007) Determination of metal content in wild edible mushrooms species from region of Greece. J Food Compos Anal 20:480–486
Pandolfini T, Gremigni P, Gabbrielli R (1997) Biomonitoring of soil health by plants. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CAB, New York, pp 325–347
Pawlowska TE, Charvat I (2004) Heavy metal stress and developmental patterns in arbuscular mycorrhizal fungi. Appl Environ Microbiol 70:6643–6649
Pawlowska TE, Blaszkowski J, Rühling A (1996) The mycorrhizal status of plants colonizing a calamine spoil mound in southern Poland. Mycorrhiza 6:499–505
Pennanen T, Frostegård A, Fritze H, Bååth E (1996) Phospholipid fatty acid composition and heavy metal tolerance of soil microbial communities along two heavy metal-polluted gradients in coniferous forests. Appl Environ Microbiol 62:420–428
Rahmanian M, Khodaverdiloo H, Rezaee Danesh Y, Rasouli Sadaghiani MH (2011) Effects of heavy metal resistant soil microbes inoculation and soil Cd concentration on growth and metal uptake of millet, couch grass and alfalfa. Afr J Microbiol Res 5:403–410
Rajapaksha R, Tobor-Kaplon MA, Bååth E (2004) Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 70:2966–2973
Ranjard L, Nazaret S, Gourbiere F, Thioulouse J, Linet P, Richaume A (2000) A soil microscale study to reveal the heterogeneity of Hg (II) impact on indigenous bacteria by quantification of adapted phenotypes and analysis of community DNA fingerprints. FEMS Microbiol Ecol 31: 107–115
Renella G, Mench M, van der Lelie D, Pietramellara G, Ascher J, Ceccherini MT, Landi L, Nannipieri P (2004) Hydrolase activity, microbial biomass and community structure in long-term Cd-contaminated soils. Soil Biol Biochem 36:443–451
Romandini P, Tallandini L, Beltramini M, Salvato B, Manzano M (1992) Effects of copper and cadmium on growth, superoxide dismutase and catalase activities in different yeast strains. Comp Biochem Physiol 103C:255–262
Rufyikiri G, Huysmans L, Wannijin J, Hees MV, Leyval C, Jakobsen I (2004) Arbuscular mycorrhizal fungi can decrease the uptake of uranium by subterranean clover grown at high levels of uranium in soil. Environ Pollut 130:427–436
Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49: 643–668
Sandaa RA, Torsvik V, Enger O, Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251
Saxena PK, Raj SK, Dan T, Perras MR, Vettakkorumakankav NN (1999) Phytoremediation of heavy metal contaminated and polluted soils. In: Prasad MNV, Hagemayr J (eds) Heavy metal stress in plants. From molecules to ecosystems. Springer, Berlin, pp 305–329
Schnoor JL (1997) Phytoremediation. Technology evaluation report. Ground-Water Remediation Technologies Analysis Center. E Series TE-98-101
Schubler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421
Shakolnik MY (1984) Trace elements in plants. Elsevier, NewYork, pp 140–171
Sharma A, Talukdar G (1987) Effects of metals on chromosomes of higher organisms. Environ Mutagen 9:191–226
Shi W, Becker J, Bischoff M, Turco RF, Konopka AE (2002) Association of microbial community composition and activity with lead, chromium, and hydrocarbon contamination. Appl Environ Microbiol 68:3859–3866
Singh H (2006) Mycoremediation: fungal bioremediation. Wiley-Interscience, Hoboken, NJ
Smejkalova M, Mikanova O, Boruvka L (2003) Effect of heavy metal concentration on biological activity of soil microorganisms. Plant Soil Environ 49:321–326
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic and Elsevier, London
Soylak M, Saraçoğlu S, Tüzen M, Mendil D (2005) Determination of trace metals in mushroom sample from Kayseri, Turkey. Food Chem 92:649–652
Speir TW, Kettles HA, Parshotam A, Searle PL, Vlaar LNC (1995) A simple kinetic approach to derive the ecological dose value, ED(50), for the assessment of Cr(VI) toxicity to soil biological properties. Soil Biol Biochem 27:801–810
Steffens JC (1990) The heavy metal-binding peptides of plants. Annu Rev Plant Physiol 41: 553–575
Stresty EV, Madhava Rao KV (1999) Ultrastructural alterations in response to zinc and nickel stress in the root cells of pigeonpea. Environ Exp Bot 41:3–13
Svoboda L, Havličková B, Kalač P (2006) Contents of cadmium, mercury and lead in edible mushrooms growing in a historical silver-mining area. Food Chem 96:580–585
Szili-Kovács T, Anton A, Gulyás F (1999) Effect of Cd, Ni and Cu on some microbial properties of a calcareous chernozem soil. In: Kubát J (ed) Proceedings of 2nd symposium on the pathways and consequences of the dissemination of pollutants in the biosphere, Prague, pp 88–102
Thomas KW (2008) Molecular approaches in bioremediation. Curr Opin Biotechnol 19:572–578
Timmis KN, Piper DH (1999) Bacteria designed for bioremediation. Trends Biotechnol 17: 201–204
Tonin C, Vandenkoornhuyse P, Joner EJ, Straczek J, Leyval C (2001) Assessment of arbuscular mycorrhizal fungi diversity in the rhizosphere of Viola calaminaria and effect of these fungi on heavy metal uptake by clover. Mycorrhiza 10:161–168
Torslov J (1993) Comparison of bacterial toxicity tests based on growth, dehydrogenase activity and esterase activity of Pseudomonas fluorescens. Ecotoxicol Environ Saf 25:33–40
Turnau K, Ryszka P, Gianinazzi PV, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plant colonizing zinc wastes in southern Poland. Mycorrhiza 10: 169–174
Turnau K, Jurkiewicz A, Lingua G, Barea JM, Gianinazzi-Pearson V (2006) Role of arbuscular mycorrhiza and associated microorganisms in phytoremediation of heavy metal-polluted sites (chapter 13). In: Prasad MNV, Sajwan KS, Naidu R (eds) Trace elements in the environment. Biogeochemistry, biotechnology, and bioremediation. CRC, Boca Raton, FL
Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006) Assessments of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environ Microbiol 8:971–983
Van Assche F, Clijsters H (1990) Effect of metals on enzyme activity in plants. Plant Cell Environ 13:195–206
Van Veen JA, Ladd JN, Amato M (1985) Turnover of carbon and nitrogen through the microbial biomass in a sandy loam and a clay soil incubated with [14C(U)]glucose and [15N](NH4)SO4 under different moisture regimes. Soil Biol Biochem 17:747–756
Vivas A, Barea JM, Biro B, Azcon R (2006) Effectiveness of autochthonous bacterium and mycorrhizal fungus on Trifolium growth, symbiotic development and soil enzymatic activities in Zn contaminated soil. J Appl Microbiol 100:587–598
Voegelin A, Barmettler K, Kretzschmar R (2003) Heavy metal release from contaminated soils: comparison of column leaching and batch extraction results. J Environ Qual 32:865–875
Vogel-Mikus K, Pongrac P, Kump P, Necemer M, Regvar M (2006) Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake. Environ Pollut 139:362–371
Volesky B, Holan ZR (1995) Biosorption of heavy metals. Biotechnol Prog 11:235–250
Wang FY, Lin XG, Yin R (2007a) Effect of arbuscular mycorrhizal fungal inoculation on heavy metal accumulation of maize grown in a naturally contaminated soil. Int J Phytoremediation 9: 345–353
Wang FY, Lin XG, Yin R (2007b) Inoculation with arbuscular mycorrhizal fungus Acaulospora mellea decrease Cu phytoextraction by maize from Cu-contaminated soil. Pedobiologia 51: 99–109
Wang FY, Lin XG, Yin R (2007c) Role of microbial inoculation and chitosan in phytoextraction of Cu, Zn, Pb and Cd by Elsholtzia splendens – a field case. Environ Pollut 147:248–255
Wani PA, Khan MS, Zaidi A (2007a) Cadmium, chromium and copper in greengram plants. Agron Sustain Dev 27:145–153
Wani PA, Khan MS, Zaidi A (2007b) Impact of heavy metal toxicity on plant growth, symbiosis, seed yield and nitrogen and metal uptake in chickpea. Aust J Exp Agric 47:712–720
Wecks JEJ, Clisjsters HMM (1997) Zn toxicity induces oxidative stress in primary leaves of Phaseolus vulgaris. Plant Physiol Biochem 35:405–410
Weissenhorn I, Leyval C, Berthelin J (1993) Cd-tolerant arbuscular mycorrhizal (AM) fungi from heavy-metal polluted soils. Plant Soil 157:247–256
Wenzel WW, Adriano DC, Sal D, Smith R (1999) Phytoremediation: a plant-microbe-based remediation system. In: Adriano DC, Bollag JM, Frankenburger WT Jr, Sims RC (eds) Bioremediation of contaminated soils, vol 37, Agronomy monographs. ASA, CSSA, and SSSA, Madison, WI, pp 457–508
Whitfield L, Richards AJ, Rimmer DL (2004) Relationships between soil heavy metal concentration and mycorrhizal colonization in Thymus polytrichus in Northern England. Mycorrhiza 14:55–62
Winge DR et al (1985) Yeast metallothionein: sequence and metal-binding properties. J Biol Chem 260:14464–14470
Wolt J (1994) Soil solution chemistry. Wiley, New York
Yeats GW, Orchard VA, Speir TW, Hunt JL, Hermans MCC (1994) Impact of pasture contamination by copper, chromium, arsenic and timber preservative on soil biological activity. Biol Fertil Soils 18:200–208
Zarei M (2008) Diversity of arbuscular mycorrhizal fungi in heavy metal pollution soils and their roles in phytoremediation. Ph.D. dissertation in Soil Science (Soil Biology and Biotechnology), Agricultural Faculty, University of Tehran, Tehran, Iran, p 219 (In Persian with an English abstract)
Zarei M, Sheikhi J (2010) The role of arbuscular mycorrhizal fungi in phytostabilization and phytoextraction of heavy metal contaminated soils. In: Golubev IA (ed) Handbook of phytoremediation. Nova, New York
Zarei M, König S, Hempel S, Khayam Nekouei M, Savaghebi G, Buscot F (2008a) Community structure of arbuscular mycorrhizal fungi associated to Veronica rechingeri at the Anguran zinc and lead mining region. Environ Pollut 156:1277–1283
Zarei M, Saleh-Rastin N, Salehi Jouzani G, Savaghebi G, Buscot F (2008b) Arbuscular mycorrhizal abundance in contaminated soils around a zinc and lead deposit. Eur J Soil Biol 44:381–391
Zarei M, Hempel S, Wubet T, Schäfer T, Savaghebi G, Jouzani GS, Nekouei MK, Buscot F (2010) Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environ Pollut 158:2757–2765
Zelles L, Bai QY, Ma RX, Rackwitz R, Winter K, Beese F (1994) Microbial biomass, metabolic activity and nutritional status determined from fatty acid patterns and poly-hydroxybutyrate in agriculturally-managed soils. Soil Biol Biochem 26:439–446
Zhu YL, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamyl-cysteine synthetase. Plant Physiol 121:1169–1176
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Sepehri, M., Khodaverdiloo, H., Zarei, M. (2013). Fungi and Their Role in Phytoremediation of Heavy Metal-Contaminated Soils. In: Goltapeh, E., Danesh, Y., Varma, A. (eds) Fungi as Bioremediators. Soil Biology, vol 32. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33811-3_14
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