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Symbioses of Plants with Rhizobia and Mycorrhizal Fungi in Heavy Metal-Contaminated Tropical Soils

  • Chapter
Heavy Metal Contamination of Soils

Part of the book series: Soil Biology ((SOILBIOL,volume 44))

Abstract

Symbioses of plants with rhizobia and mycorrhizal fungi have been poorly studied in heavy metal-contaminated tropical soils. Studies found were mainly in areas subject to Zn processing, coal and gold mining activities and sewage sludge application. Although no data were found about the occurrence of rhizobia in these soils, tolerance of rhizobia from diverse origins (plant species and ecosystems) revealed strains with high tolerance to Zn, Cd and Cu. Cupriavidus necator, recently described as a nitrogen-fixing legume symbiont, is among the high-tolerant species. The arbuscular mycorrhizal fungi (AMF) genera most commonly reported in heavy metal (HM)-contaminated areas were Glomus and Acaulospora. Some tropical legume trees have been identified as promising for programmes to recover soils degraded by excess HMs, such as Enterolobium contortisiliquum and Acacia mangium, which are able to form an efficient symbiosis with Bradyrhizobium, Mimosa caesalpiniaefolia and Leucaena leucocephala, which form symbioses with Cupriavidus necator. AMF were shown to improve the tolerance of hosting plants to As in contaminated soils. Leguminous species had a low As translocation index from the roots to shoots when inoculated with AMF species.

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References

  • Andrade SA, Silveira AP (2008) Mycorrhiza influence on maize development under Cd stress and P supply. Braz J Plant Physiol 20(1):39–50

    Google Scholar 

  • Andrade MG, Lima AST, Melo WJ, Santos EJ, Herrmann AB (2014) Elementos-traço em dois latossolos após aplicações anuais de lodo de esgoto por treze anos. Semina Ciências Agrárias 35(1):135–148

    Google Scholar 

  • Andrade S, Abreu C, Abreu M, Silveira A (2003) Interação de chumbo, da saturação por bases do solo e de micorriza arbuscular no crescimento e nutrição mineral da soja. Rev Bras Ciênc Solo 27(5):945–954

    CAS  Google Scholar 

  • Andrade S, Abreu C, De Abreu M, Silveira A (2004) Influence of lead additions on arbuscular mycorrhiza and Rhizobium symbioses under soybean plants. Soil Ecol Appl 26(2):123–131

    Google Scholar 

  • Andrade SAL, Jorge RA, Silveira APD (2005) Cadmium effect on the association of jackbean (Canavalia ensiformis) and arbuscular mycorrhizal fungi. Sci Agric 62(4):389–394

    Google Scholar 

  • Andrade SAL, Silveira APD, Jorge RA, Abreu MF (2008) Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. Int J Phytoremediat 10(1):1–13

    Google Scholar 

  • Andrade S, Silveira A, Mazzafera P (2010) Arbuscular mycorrhiza alters metal uptake and the physiological response of Coffea arabica seedlings to increasing Zn and Cu concentrations in soil. Sci Total Environ 408(22):5381–5391

    CAS  PubMed  Google Scholar 

  • Angle JS, McGrath SP, Chaudri AM, Chaney RL, Giller KE (1993) Inoculation effects on legumes grown in soil previously treated with sewage sludge. Soil Biol Biochem 25(5):575–580

    Google Scholar 

  • dos Anjos ARM, Mattiazzo ME (2000) Metais pesados em plantas de milho cultivadas em Latossolos repetidamente tratados com biossólido. Sci Agric 57(4):769–776

    Google Scholar 

  • Appel C, Ma L (2002) Concentration, pH, and surface charge effects on cadmium and lead sorption in three tropical soils. J Environ Qual 31(2):581–589

    CAS  PubMed  Google Scholar 

  • Araújo SR, Demattê JA, Vicente S (2014) Soil contaminated with chromium by tannery sludge and identified by vis-NIR-mid spectroscopy techniques. Int J Remote Sens 35(10):3579–3593

    Google Scholar 

  • Arriagada C, Pereira G, García-Romera I, Ocampo J (2010) Improved zinc tolerance in Eucalyptus globulus inoculated with Glomus deserticola and Trametes versicolor or Coriolopsis rigida. Soil Biol Biochem 42(1):118–124

    CAS  Google Scholar 

  • Atafar Z, Mesdaghinia A, Nouri J, Homaee M, Yunesian M, Ahmadimoghaddam M, Mahvi AH (2010) Effect of fertilizer application on soil heavy metal concentration. Environ Monit Assess 160(1–4):83–89

    CAS  PubMed  Google Scholar 

  • Bigarelli W, Alves F (1998) Minas Gerais: Mantendo-se como líder na mineração brasileira. Brasil Miner 162:14–18

    Google Scholar 

  • Cabral L, Siqueira JO, Soares CRFS, Pinto JEBP (2010) Retenção de metais pesados em micélio de fungos micorrízicos arbusculares. Quim Nova 33(1):25–29

    CAS  Google Scholar 

  • Cai Q-Y, Mo C-H, Wu Q-T, Zeng Q-Y, Katsoyiannis A (2007) Concentration and speciation of heavy metals in six different sewage sludge-composts. J Hazard Mater 147(3):1063–1072

    CAS  PubMed  Google Scholar 

  • Camilotti F, Silva ARB, Marques MO (2012) Biomass and yield of peanut grown on tropical soil amended with sewage sludge contaminated with lead. Appl Soil Ecol 2012:1–6

    Google Scholar 

  • Cardoso E, Navarro R, Nogueira M (2002) Manganês e germinação de esporos de fungos micorrízicos arbusculares in vitro. Rev Bras Ciênc Solo 26(3):795–799

    CAS  Google Scholar 

  • Cardoso E, Navarro R, Nogueira M (2003) Absorção e translocação de manganês por plantas de soja micorrizadas, sob doses crescentes deste nutriente. Rev Bras Ciênc Solo 27(3):415–423

    CAS  Google Scholar 

  • Carneiro MAC, Siqueira JO, Moreira FMS (2001) Estabelecimento de plantas herbáceas em solo com contaminação de metais pesados e inoculação de fungos micorrízicos arbusculares. Pesquisa Agropecuária Brasileira 36(12):1443–1452

    Google Scholar 

  • Castaldi P, Melis P, Silvetti M, Deiana P, Garau G (2009) Influence of pea and wheat growth on Pb, Cd, and Zn mobility and soil biological status in a polluted amended soil. Geoderma 151(3):241–248

    CAS  Google Scholar 

  • Chaudhary P, Dudeja S, Kapoor K (2004) Effectivity of host-Rhizobium leguminosarum symbiosis in soils receiving sewage water containing heavy metals. Microbiol Res 159(2):121–127

    CAS  PubMed  Google Scholar 

  • Collard J-M, Corbisier P, Diels L, Dong Q, Jeanthon C, Mergeay M, Taghavi S, Van Der Lelie D, Wilmotte A, Wuertz S (1994) Plasmids for heavy metal resistance in Alcaligenes eutrophus CH34: mechanisms and applications. FEMS Microbiol Rev 14(4):405–414

    CAS  PubMed  Google Scholar 

  • Comte S, Guibaud G, Baudu M (2008) Biosorption properties of extracellular polymeric substances (EPS) towards Cd, Cu and Pb for different pH values. J Hazard Mater 151(1):185–193

    CAS  PubMed  Google Scholar 

  • CONAMA (2009) Dispõe sobre critérios e valores orientadores de qualidade do solo quanto à presença de substâncias químicas e estabelece diretrizes para o gerenciamento ambiental de áreas contaminadas por essas substâncias em decorrência de atividades antrópicas. Resolução 420. Diário Oficial da União, Brasília

    Google Scholar 

  • Cook WJ, Kar SR, Taylor KB, Hall LM (1998) Crystal structure of the cyanobacterial metallothionein repressor SmtB: a model for metalloregulatory proteins. J Mol Biol 275(2):337–346

    CAS  PubMed  Google Scholar 

  • 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 Tot Environ 406(1):154–160

    CAS  Google Scholar 

  • Cunha KP, do Nascimento CW, Pimentel RM, Ferreira CP (2008) Cellular localization of cadmium and structural changes in maize plants grown on a cadmium contaminated soil with and without liming. J Hazard Mater 160(1):228–234

    PubMed  Google Scholar 

  • Del Val C, Barea J, Azcon-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65(2):718–723

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dias-Junior H, Moreira FMS, Siqueira J, Silva R (1998) Metais pesados, densidade e atividade microbiana em solo contaminado por rejeitos de indústria de zinco. Rev Bras Ciênc Solo 22(4)

    Google Scholar 

  • Dœlsch E, Deroche B, Van de Kerchove V (2006) Impact of sewage sludge spreading on heavy metal speciation in tropical soils (Réunion, Indian Ocean). Chemosphere 65(2):286–293

    PubMed  Google Scholar 

  • Fernandes AR, de Paiva H, de Carvalho JG, de Miranda JRP (2007a) Crescimento e absorção de nutrientes por mudas de freijó (Cordia goeldiana Huber) em função de doses de fósforo e de zinco. Revista Árvore 31(4):599–608

    CAS  Google Scholar 

  • Fernandes R, Luz W, Fontes M, Fontes L (2007b) Avaliação da concentração de metais pesados em áreas olerícolas no estado de Minas Gerais. Revista Brasileira de Engenharia Agricola e Ambiental 11(1):81–93

    Google Scholar 

  • Ferreira PAA (2014) Tolerância de Cupriavidus necator a cádmio e zinco e sua eficiência simbiótica em leguminosas. Universidade Federal de Lavras, Lavras, Tese

    Google Scholar 

  • Ferreira PAA, Bomfeti CA, Silva Júnior R, Soares BL, Soares CRFS, Souza Moreira FMS (2012) Eficiência simbiótica de estirpes de Cupriavidus necator tolerantes a zinco, cádmio, cobre e chumbo. Pesquisa Agropecuária Brasileira 47(1):85–95

    Google Scholar 

  • Ferreira PAA, Lopes G, Bomfeti CA, de Oliveira Longatti SM, de Sousa Soares CRF, Guilherme LRG, de Souza Moreira FMS (2013) Leguminous plants nodulated by selected strains of Cupriavidus necator grow in heavy metal contaminated soils amended with calcium silicate. World J Microbiol Biotechnol 29(11):2055–2066

    CAS  Google Scholar 

  • Florentino LA, Guimarães AP, Rufini M, da Silva K, de Moreira FMS (2009) Sesbania virgata stimulates the occurrence of its microsymbiont in soils but does not inhibit microsymbionts of other species. Sci Agric 66(5):667–676

    Google Scholar 

  • Fontes MPF, Gomes PC (2003) Simultaneous competitive adsorption of heavy metals by the mineral matrix of tropical soils. Appl Geochem 18(6):795–804

    CAS  Google Scholar 

  • Fred EB, Waksman SA (1928) Laboratory manual of general microbiology. Book Company, New York

    Google Scholar 

  • Gadd GM, White C (1993) Microbial treatment of metal pollution—a working biotechnology? Trends Biotechnol 11(8):353–359

    CAS  PubMed  Google Scholar 

  • Gattai G, Pereira S, Costa C, Lima C, Maia L (2011) Microbial activity, arbuscular mycorrhizal fungi and inoculation of wood plants in lead contaminated soil. Braz J Microbiol 42:859–867

    PubMed Central  CAS  PubMed  Google Scholar 

  • Germaine KJ, McGuinness M, Dowling DN (2013) Improving phytoremediation through plant‐associated bacteria. In: Brujin F (ed) Molecular microbial ecology of the rhizosphere: vol 1 and 2. Wiley, Hoboken, pp 961–973

    Google Scholar 

  • Ghorbani N, Salehrastin N, Moeini A (2002) Heavy metals affect the microbial populations and their activities. Proc 17th World Congr. Soil Sci 2234:1–11

    Google Scholar 

  • Giller KE, Witter E, Mcgrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30(10):1389–1414

    CAS  Google Scholar 

  • Gonçalves Júnior AC, Luchese EB, Lenzi E (2000) Avaliação da fitodisponibilidade de cádmio, chumbo e crômio, em soja cultivada em Latossolo Vermelho escuro tratado com fertilizantes comerciais. Quím Nova 23(2):173–177

    Google Scholar 

  • Gonzalez-Chavez C, D’Haen J, Vangronsveld J, Dodd J (2002a) Copper sorption and accumulation by the extraradical mycelium of different Glomus spp. (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240(2):287–297

    CAS  Google Scholar 

  • Gonzalez-Chavez M, Carrillo-Gonzalez R, Gutierrez-Castorena M (2009) Natural attenuation in a slag heap contaminated with cadmium: the role of plants and arbuscular mycorrhizal fungi. J Hazard Mater 161(2):1288–1298

    CAS  PubMed  Google Scholar 

  • Gonzalez-Chavez M, Carrillo-Gonzalez R, Wright S, Nichols K (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130(3):317–323

    CAS  PubMed  Google Scholar 

  • Gonzalez-Chavez C, Harris P, Dodd J, Meharg A (2002b) Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytol 155(1):163–171

    CAS  Google Scholar 

  • Grazziotti P, Siqueira J, Moreira FMS, Carvalho D (2001) Efeito de Zn, Cd e Cu no comportamento de fungos ectomicorrízicos em meio de cultura. Rev Bras Ciênc Solo 25(4):831–837

    CAS  Google Scholar 

  • Hasan S, Hayat S, Ali B, Ahmad A (2008) 28-Homobrassinolide protects chickpea (Cicer arietinum) from cadmium toxicity by stimulating antioxidants. Environ Pollut 151(1):60–66

    CAS  PubMed  Google Scholar 

  • Huang S-W, Jin J-Y (2008) Status of heavy metals in agricultural soils as affected by different patterns of land use. Environ Monit Assess 139(1–3):317–327

    CAS  PubMed  Google Scholar 

  • Ibekwe A, Angle J, Chaney R, Van Berkum P (1995) Sewage sludge and heavy metal effects on nodulation and nitrogen fixation of legumes. J Environ Qual 24(6):1199–1204

    CAS  Google Scholar 

  • Lins CEL, Cavalcante UMT, Sampaio EV, Messias AS, Maia LC (2006) Growth of mycorrhized seedlings of Leucaena leucocephala (Lam.) de Wit. in a copper contaminated soil. Appl Soil Ecol 31(3):181–185

    Google Scholar 

  • Kabata-Pendias A (2011) Trace elements in soils and plants, 4th edn. CRC, Boca Raton

    Google Scholar 

  • Kazy SK, Sar P, Singh S, Sen AK, D’Souza S (2002) Extracellular polysaccharides of a copper-sensitive and a copper-resistant Pseudomonas aeruginosa strain: synthesis, chemical nature and copper binding. World J Microbiol Biotechnol 18(6):583–588

    CAS  Google Scholar 

  • Khairiah J, Lim K, Ahmad-Mahir R, Ismail B (2006) Heavy metals from agricultural soils from cameron highlands, pahang, and cheras, Kuala Lumpur, Malaysia. Bull Environ Contam Toxicol 77(4):608–615

    CAS  PubMed  Google Scholar 

  • Klauberg-Filho O, Siqueira J, Moreira FMS (2002) Fungos micorrízicos arbusculares em solos de área poluída com metais pesados. Rev Bras Ciênc Solo 26(1):125–134

    CAS  Google Scholar 

  • Ladeira ACQ, Ciminelli VST, Nepomuceno AL (2002) Seleção de solos para a imobilização de arsênio. Rem Rev Esc Minas 55(3):215–221

    Google Scholar 

  • Ledin M, Krantz-Rülcker C, Allard B (1996) Zn, Cd and Hg accumulation by microorganisms, organic and inorganic soil components in multi-compartment systems. Soil Biol Biochem 28(6):791–799

    CAS  Google Scholar 

  • Lovley DR, Widman PK, Woodward JC, Phillips E (1993) Reduction of uranium by cytochrome c3 of Desulfovibrio vulgaris. Appl Environ Microbiol 59(11):3572–3576

    PubMed Central  CAS  PubMed  Google Scholar 

  • Macnair MR (1993) The genetics of metal tolerance in vascular plants. New Phytol 124(4):541–559

    CAS  Google Scholar 

  • Maftoun M, Moshiri F, Karimian N, Ronaghi A (2005) Effects of two organic wastes in combination with phosphorus on growth and chemical composition of spinach and soil properties. J Plant Nutr 27(9):1635–1651

    Google Scholar 

  • Marques TS, Moreira FMS, Siqueira J (2000) Crescimento e teor de metais de muda de especies arboreas cultivadas em solo contaminado com metais pesados. Pesquisa Agropecuária Brasileira 35:121–132

    Google Scholar 

  • Mårtensson A, Witter E (1990) Influence of various soil amendments on nitrogen-fixing soil microorganisms in a long-term field experiment, with special reference to sewage sludge. Soil Biol Biochem 22(7):977–982

    Google Scholar 

  • Matsuda A, Moreira FMS, Siqueira J (2002a) Sobrevivência de Bradyrhizobium e Azorhizobium em misturas de solo contaminadas com metais pesados. Rev Bras Ciênc Solo 26(1):249–256

    CAS  Google Scholar 

  • Matsuda A, Moreira FMS, Siqueira JO (2002b) Tolerância de rizóbios de diferentes procedências ao zinco, cobre e cádmio. Pesquisa Agropecuária Brasileira 37(3):343–355

    Google Scholar 

  • McBride M (1989) Reactions controlling heavy metal solubility in soils. Advances in soil science. Springer, New York, pp 1–56

    Google Scholar 

  • Meharg AA (2003) The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycol Res 107(11):1253–1265

    CAS  PubMed  Google Scholar 

  • Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42(7):741–775

    CAS  Google Scholar 

  • Mergulhão A, Oliveira J, Burity H, Maia L (2007) Potencial de infectividade de fungos micorrízicos arbusculares em áreas nativas e impactadas por mineração gesseira no semi-árido brasileiro. Hoehnea 34(3):341–348

    Google Scholar 

  • Mishra VK, Upadhyay AR, Tripathi B (2009) Bioaccumulation of heavy metals and two organochlorine pesticides (DDT and BHC) in crops irrigated with secondary treated waste water. Environ Monit Assess 156(1–4):99–107

    CAS  PubMed  Google Scholar 

  • Moreira FMS, Cruz L, Miana de Faria S, Marsh T, Martínez-Romero E, Oliveira Pedrosa F, Maria Pitard R, Peter W, Young J (2006) Azorhizobium doebereinerae sp. Nov. Microsymbiont of Sesbania virgata (Caz.) Pers. Syst Appl Microbiol 29(3):197–206

    CAS  Google Scholar 

  • Niu H, Xu XS, Wang JH, Volesky B (1993) Removal of lead from aqueous solutions by Penicillium biomass. Biotechnol Bioeng 42(6):785–787

    CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49(1):249–279

    CAS  Google Scholar 

  • Nogueira AV (1996) As micorrizas e o excesso de metais. In: Siqueira JO (ed) Avanços em fundamentos e aplicação de micorrizas. Universidade Federal de Lavras, Lavras, pp 135–174

    Google Scholar 

  • Nogueira MA, Cardoso EJBN (2003) Mycorrhizal effectiveness and manganese toxicity in soybean as affected by soil type and endophyte. Sci Agric 60(2):329–335

    CAS  Google Scholar 

  • Nogueira MA, Magalhães GC, Cardoso EJ (2004) Manganese toxicity in mycorrhizal and phosphorus-fertilized soybean plants. J Plant Nutr 27(1):141–156

    CAS  Google Scholar 

  • Nogueira M, Nehls U, Hampp R, Poralla K, Cardoso E (2007) Mycorrhiza and soil bacteria influence extractable iron and manganese in soil and uptake by soybean. Plant Soil 298(1–2):273–284

    CAS  Google Scholar 

  • Nogueira TAR, Franco A, He Z, Braga VS, Firme LP, Abreu-Junior CH (2013) Short-term usage of sewage sludge as organic fertilizer to sugarcane in a tropical soil bears little threat of heavy metal contamination. J Environ Manage 114:168–177

    CAS  PubMed  Google Scholar 

  • Obbard J (2001) Ecotoxicological assessment of heavy metals in sewage sludge amended soils. Appl Geochem 16(11):1405–1411

    CAS  Google Scholar 

  • Ortega-Larrocea M, Siebe C, Estrada A, Webster R (2007) Mycorrhizal inoculum potential of arbuscular mycorrhizal fungi in soils irrigated with wastewater for various lengths of time, as affected by heavy metals and available P. Appl Soil Ecol 37(1):129–138

    Google Scholar 

  • Parkpain P, Sreesai S, Delaune R (2000) Bioavailability of heavy metals in sewage sludge-amended Thai soils. Water Air Soil Pollut 122(1–2):163–182

    CAS  Google Scholar 

  • Parkpian P, Leong ST, Laortanakul P, Thunthaisong N (2003) Regional monitoring of lead and cadmium contamination in a tropical grazing land site, Thailand. Environ Monit Assess 85(2):157–173

    CAS  PubMed  Google Scholar 

  • Pierangeli M, Guilherme L, Curi N, Anderson S, Lima J (2004) Adsorção e dessorção de cádmio, cobre e chumbo por amostras de Latossolos pré-tratadas com fósforo. Rev Bras Ciênc Solo 28(2):377–384

    CAS  Google Scholar 

  • Purchase D, Miles RJ, Young TW (1997) Cadmium uptake and nitrogen fixing ability in heavy‐metal‐resistant laboratory and field strains of Rhizobium leguminosarum biovar trifolii. FEMS Microbiol Ecol 22(1):85–93

    CAS  Google Scholar 

  • Rangel OJP, Silva CA, Bettiol W, Dynia JF (2006) Efeito de aplicações de lodos de esgoto sobre os teores de metais pesados em folhas e grãos de milho. Rev Bras Ciênc Solo 30(3):583–594

    Google Scholar 

  • de Rangel WM, Schneider J, de Costa ETS, Soares CRFS, Guilherme LRG, de Moreira FMS (2014) Phytoprotective effect of arbuscular mycorrhizal fungi species against arsenic toxicity in tropical leguminous species. Int J Phytoremediat 16:840–858

    CAS  Google Scholar 

  • Raman N, Sambandan K (1998) Distribution of VAM fungi in tannery effluent polluted soils of Tamil Nadu, India. Bull Environ Contam Toxicol 60(1):42–150

    Google Scholar 

  • Rashid A, Ayub N, Ahmad T, Gul J, Khan AG (2009) Phytoaccumulation prospects of cadmium and zinc by mycorrhizal plant species growing in industrially polluted soils. Environ Geochem Health 31(1):91–98

    CAS  PubMed  Google Scholar 

  • Rensing C, Sun Y, Mitra B, Rosen BP (1998) Pb (II)-translocating P-type ATPases. J Biol Chem 273(49):32614–32617

    CAS  PubMed  Google Scholar 

  • Rillig MC, Steinberg PD (2002) Glomalin production by an arbuscular mycorrhizal fungus: a mechanism of habitat modification? Soil Biol Biochem 34(9):1371–1374

    CAS  Google Scholar 

  • Santos F, Amaral Sobrinho N, Mazur N (2003) Conseqüências do manejo do solo na distribuição de metais pesados em um agrossistema com feijão de vagem (Phaseolus vulgaris L.). Rev Bras Ciênc Solo 27(1):191–198

    CAS  Google Scholar 

  • Santos JV, Melo Rangel W, Guimaraes AA, Jaramillo PMD, Rufini M, Marra LM, López MV, Silva MAP, Soares CRFS, Souza Moreira FMS (2013) Soil biological attributes in arsenic-contaminated gold mining sites after revegetation. Ecotoxicology 22(10):1526–1537

    PubMed  Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal‐induced oxidative stress and protection by mycorrhization. J Exp Bot 53(372):1351–1365

    PubMed  Google Scholar 

  • Scott J, Palmer S (1990) Sites of cadmium uptake in bacteria used for biosorption. Appl Microbiol Biotechnol 33(2):221–225

    CAS  PubMed  Google Scholar 

  • Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58

    CAS  PubMed  Google Scholar 

  • Sharma RK, Agrawal M, Marshall FM (2009) Heavy metals in vegetables collected from production and market sites of a tropical urban area of India. Food Chem Toxicol 47(3):583–591

    CAS  PubMed  Google Scholar 

  • Silva GA, Trufem SFB, Júnior OJS, Maia LC (2005) Arbuscular mycorrhizal fungi in a semiarid copper mining area in Brazil. Mycorrhiza 15(1):47–53

    PubMed  Google Scholar 

  • da Silva G, Maia LC, da Silva F, Lima PCF (2001) Potencial de infectividade de fungos micorrízicos arbusculares oriundos de área de caatinga nativa e degradada por mineração, no Estado da Bahia, Brasil. Rev Bras Bot 24(2):135–143

    Google Scholar 

  • Silva K, Florentino LA, Silva KB, Brandt E, Vandamme P, Souza Moreira FMS (2012) Cupriavidus necator isolates are able to fix nitrogen in symbiosis with different legume species. Syst Appl Microbiol 35(3):175–182

    PubMed  Google Scholar 

  • Silva LF, Fdez-Ortiz de Vallejuelo S, Martinez-Arkarazo I, Castro K, Oliveira ML, Sampaio CH, de Brum IA, de Leão FB, Taffarel SR, Madariaga JM (2013) Study of environmental pollution and mineralogical characterization of sediment rivers from Brazilian coal mining acid drainage. Sci Total Environ 447:169–178

    CAS  PubMed  Google Scholar 

  • de Silva MLS, Vitti GC, Trevizam AR (2007) Concentração de metais pesados em grãos de plantas cultivadas em solo com diferentes níveis de contaminação. Pesq agropec bras Brasília 42(4):527–535

    Google Scholar 

  • Silver S, Phung LT (1996) Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50(1):753–789

    CAS  PubMed  Google Scholar 

  • Siqueira J, Pereira M, Simão J, Moreira FMS (1999a) Efeito da formononetina (7 Hidroxi, 4″ metoxi Isoflavona) na colonização micorrízica e crescimento do milho em solo contendo excesso de metais pesados. Rev Bras Ciênc Solo 23(3):561–567

    CAS  Google Scholar 

  • Siqueira J, Pouyú E, Moreira FMS (1999b) Micorrizas arbusculares no crescimento pós-transplantio de mudas de árvores em solo com excesso de metais pesados. Rev Bras Ciênc Solo 23:569–580

    Google Scholar 

  • Soares C, Siqueira JO, de Carvalho JG, Guilherme LRG (2006) Micorriza arbuscular e nutrição fosfática na toxidez de zinco para a trema [Trema micrantha (L.) Blum]. Rev Bras Ciênc Solo 30(4):665–675

    CAS  Google Scholar 

  • Soares PSM, Borma LDS (2002) Drenagem ácida e gestão de resíduos sólidos de mineração. In: Trindade R, Barbosa Filho O (eds) Extração de Ouro: Princípios, Tecnologia e Meio Ambiente. Centro de Tecnologia Mineral—CETEM, Ministério da Ciência e Tecnologia, Rio de Janeiro, pp 242–266

    Google Scholar 

  • Soumare M, Tack F, Verloo M (2003) Distribution and availability of iron, manganese, zinc, and copper in four tropical agricultural soils. Commun Soil Sci Plant Anal 34(7–8):1023–1038

    CAS  Google Scholar 

  • Thawornchaisit U, Polprasert C (2009) Evaluation of phosphate fertilizers for the stabilization of cadmium in highly contaminated soils. J Hazard Mater 165(1):1109–1113

    CAS  PubMed  Google Scholar 

  • Trannin I, FMS M, Siqueira J, Lima A (2001a) Tolerância de estirpes e isolados de Bradyrhizobium e de Azorhizobium a zinco, cádmio e cobre in vitro. Rev Bras Ciênc Solo 25(2):305–316

    CAS  Google Scholar 

  • Trannin I, Moreira FMS, Siqueira J (2001b) Crescimento e nodulação de Acacia mangium, Enterolobium contortisiliquum e Sesbania virgata em solo contaminado com metais pesados. Rev Bras Ciênc Solo 25(3):743–753

    CAS  Google Scholar 

  • Uchimiya M, Wartelle LH, Boddu VM (2012) Sorption of triazine and organophosphorus pesticides on soil and biochar. J Agric Food Chem 60(12):2989–2997

    CAS  PubMed  Google Scholar 

  • Udom B, Mbagwu J, Adesodun J, Agbim N (2004) Distributions of zinc, copper, cadmium and lead in a tropical ultisol after long-term disposal of sewage sludge. Environ Int 30(4):467–470

    CAS  PubMed  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of root-nodule bactéria, vol 15, International biological programme handbook. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Weissenhorn I, Glashoff A, Leyval C, Berthelin J (1994) Differential tolerance to Cd and Zn of arbuscular mycorrhizal (AM) fungal spores isolated from heavy metal-polluted and unpolluted soils. Plant and Soil 167(2):189–196

    CAS  Google Scholar 

  • 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(8):2757–2765

    CAS  PubMed  Google Scholar 

  • Zarei M, König S, Hempel S, Nekouei MK, 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(3):1277–1283

    CAS  PubMed  Google Scholar 

  • Zarei M, Saleh-Rastin N, Jouzani GS, Savaghebi G, Buscot F (2008b) Arbuscular mycorrhizal abundance in contaminated soils around a zinc and lead deposit. Eur J Soil Biol 44(4):381–391

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Soil Science, Federal University of Lavras (Universidade Federal de Lavras - UFLA), Caixa Postal 3037, Lavras, Minas Gerais, Brazil

    Fatima Maria de Souza Moreira, Laíze Aparecida Ferreira Vilela & Marco Aurélio Carbone Carneiro

  2. Department of Soil, Federal University of Santa Maria (Universidade Federal de Santa Maria - UFSM), Santa Maria, Rio Grande do Sul, Brazil

    Paulo Ademar Avelar Ferreira

Authors
  1. Fatima Maria de Souza Moreira
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  2. Paulo Ademar Avelar Ferreira
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  3. Laíze Aparecida Ferreira Vilela
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  4. Marco Aurélio Carbone Carneiro
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Correspondence to Fatima Maria de Souza Moreira .

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Editors and Affiliations

  1. Institut für Allgemeine Botanik und Pflanzenphysiologie, Universität Jena, Jena, Germany

    Irena Sherameti

  2. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ajit Varma

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de Souza Moreira, F.M., Ferreira, P.A.A., Vilela, L.A.F., Carneiro, M.A.C. (2015). Symbioses of Plants with Rhizobia and Mycorrhizal Fungi in Heavy Metal-Contaminated Tropical Soils. In: Sherameti, I., Varma, A. (eds) Heavy Metal Contamination of Soils. Soil Biology, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-14526-6_12

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