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Heavy metals and soil microbes

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Abstract

Heavy metal pollution is a global issue due to health risks associated with metal contamination. Although many metals are essential for life, they can be harmful to man, animal, plant and microorganisms at toxic levels. Occurrence of heavy metals in soil is mainly attributed to natural weathering of metal-rich parent material and anthropogenic activities such as industrial, mining, agricultural activities. Here we review the effect of soil microbes on the biosorption and bioavailability of heavy metals; the mechanisms of heavy metals sequestration by plant and microbes; and the effects of pollution on soil microbial diversity and activities. The major points are: anthropogenic activities constitute the major source of heavy metals in the environment. Soil chemistry is the major determinant of metal solubility, movement and availability in the soil. High levels of heavy metals in living tissues cause severe organ impairment, neurological disorders and eventual death. Elevated levels of heavy metals in soils decrease microbial population, diversity and activities. Nonetheless, certain soil microbes tolerate and use heavy metals in their systems; as such they are used for bioremediation of polluted soils. Soil microbes can be used for remediation of contaminated soils either directly or by making heavy metals bioavailable in the rhizosphere of plants. Such plants can accumulate 100 mg g−1 Cd and As; 1000 mg g−1 Co, Cu, Cr, Ni and 10,000 mg g−1 Pb, Mn and Ni; and translocate metals to harvestable parts. Microbial activity changes soil physical properties such as soil structure and biochemical properties such as pH, soil redox state, soil enzymes that influence the solubility and bioavailability of heavy metals. The concept of ecological dose (ED50) and lethal concentration (LC50) was developed in response to the need to easily quantify the influence of pollutants on microbial-mediated ecological processes in various ecosystems.

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Fig. 1
Fig. 2
Fig. 3

Modified from Burkhardt et al. (2010)

Fig. 4

(Adapted from Ahmad et al. 2012 with permission)

Fig. 5

(Adapted from Turpeinen 2002)

Fig. 6

Adapted from Vig et al. (2003)

Fig. 7

(Adapted from Kamaludeen and Ramasamy 2008 with permission)

Fig. 8

(Adapted from Göhre and Paszkowski 2006 with permission)

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References

  • Abdousalam A (2010) Effect of heavy metals on soil microbial processes and population. Egypt Acad J Biol Sci 2:9–14

    Google Scholar 

  • Abdu N (2010) Availability, transfer and balances of heavy metals in urban agriculture of West Africa. Kassel University Press GmbH, Kassel, Germany. 140pp. ISBN 978-3-89958-957-3

  • Abdu N, Abdulkadir A, Agbenin JO, Buerkert A (2011a) Vertical distribution of heavy metals in wastewater-irrigated vegetable garden soils of three West African cities. Nutr Cycl Agroecosyst 89:387–397. doi:10.1007/s10705-10-9403-3

    Article  CAS  Google Scholar 

  • Abdu N, Agbenin JO, Buerkert A (2011b) Geochemical assessment, distribution and dynamics of trace metals in urban agricultural soils under long-term wastewater irrigation in Kano, northern Nigeria. J Plant Nutr Soil Sci 173(3):447–458. doi:10.1002/jpln.201000333

    Article  CAS  Google Scholar 

  • Adriano DC (2001) Trace elements in terrestrial environments. Biogeochemistry, bioavailability, and risks of metals. Springer, New York

    Google Scholar 

  • Agbenin JO (2002) Lead in a Nigerian savanna soil under long-term cultivation. Sci Total Environ 286:1–14. doi:10.1016/S0048-9697(01)00917-2

    Article  CAS  Google Scholar 

  • Ahmad I, Ahmad S, Inam A, Samullah A (2001) Metal and antibiotic resistance traits in Bradyrhizobium sp. (cajanus) isolated from soils receiving oil refinery waste water. World J Micro Biol Biotechnol 17:379–384. doi:10.1023/A:1016762613272

    Article  CAS  Google Scholar 

  • Ahmad I, Hayatu S, Ahmad S, Inam A, Samullah A (2005) Effect of heavy metals on survival of certain groups of indigenous soil microbial population. J Appl Sci Environ Manag 9:115–121

    Google Scholar 

  • Ahmad E, Zaidi A, Khan MS, Oves M (2012) Heavy metal toxicity to symbiotic nitrogen-fixing microorganism and host legumes. In: Zaidi A et al (eds) Toxicity of heavy metals to legumes and bioremediation. Springer, Wien. doi:10.1007/978-3-7091-0730-0_2

    Chapter  Google Scholar 

  • Allegretti P, Furlong J, Donati E (2006) The role of higher polythionates in the reduction of chromium (VI) by Acidithiobacillus and Thiobacillus cultures. J Biotechnol 122:55–61. doi:10.1016/j.jbiotec.2005.08.031

    Article  CAS  Google Scholar 

  • Alloway BJ (1995) Heavy metals in soils. Wiley, New York

    Google Scholar 

  • Anand M, Ma K, Okonski A, Lenin S, McGrath SP (2003) Characterizing biocomplexity and soil microbial dynamics along a smelter-damage landscape gradient. Sci Total Environ 311:247–259. doi:10.1016/S0048-9697(03)00058-5

    Article  CAS  Google Scholar 

  • Ayuke FO (2010) Soil macrofauna functional groups and their effects on soil structure, as related to agricultural management practices across agroecological zones of sub-Saharan Africa. PhD thesis, Wageningen University, The Netherlands, pp 41–64

  • Baath E (1989) Effect of heavy metals in soil on microbial processes and populations: a review. Water Air Soil Pollut 47:335–379. doi:10.1007/BF00279331

    Article  CAS  Google Scholar 

  • Babich H, Bewley RJF, Stotzky G (1983) Application of the ecological dose concept to the impact of heavy metals on some microbe-mediated ecological processes. Arch Environ Toxicol 12:421–426. doi:10.1007/BF01057585

    Article  CAS  Google Scholar 

  • Bach EM, Baer SG, Meyer CK, Six J (2010) Soil texture affects soil microbial and structural recovery during grassland restoration. Soil Biol Biochem 42:2182–2191. doi:10.1016/j.soilbio.2010.08.014

    Article  CAS  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 155–177

    Google Scholar 

  • Baker AJM, Reeves RD, McGrath SP (1991) In situ decontamination of heavy metal polluted soils using crops of metal-accumulating plants—a feasibility study. In: Hinchee RE, Olfenbuttel RF (eds) In situ bioreclamation. Butterworth-Heinemann, Stoneham, pp 539–544

    Google Scholar 

  • Barajas-Aceves M (2005) Comparison of different microbial biomass and activity measurement methods in metal-contaminated soils. Bioresour Technol 96:1405–1414. doi:10.1016/j.biortech.2004.09.013

    Article  CAS  Google Scholar 

  • Bardgett RD, Speir TW, Ross DJ, Yeates GW, Kettles HA (1994) Impact of pasture contamination by copper chromium and arsenic timber preservatives on soil microbial properties and nematodes. Biol Fertil Soils 18:71–79. doi:10.1007/BF00336448

    Article  CAS  Google Scholar 

  • Boonyapookana B, Parkplan P, Techapinyawat S, DeLaune RD, Jugsujinda A (2005) Phytoaccumulation of lead by sunflower (Helianthus annuus), tobacco (Nicotiana tabacum), and vetiver (Vetiveria zizanioides). J Environ Sci Heal 40:117–137. doi:10.1081/ESE-200033621

    Article  CAS  Google Scholar 

  • Brannon JM, Patrick WH (1987) Fixation, transformation, and mobilization of arsenic in sediments. Environ Sci Technol 21:450–459. doi:10.1021/es00159a005

    Article  CAS  Google Scholar 

  • Brookes PC (1995) The use of microbial parameters in monitoring soil pollution by heavy metals. Biol Fertil Soils 19:269–279. doi:10.1007/BF00336094

    Article  CAS  Google Scholar 

  • Brookes PC, McGrath SP (1984) Effect of metal toxicity and the size of the soil microbial biomass. Eur J Soil Sci 35:341–346. doi:10.1111/j.1365-2389.1984.tb00288.x

    Article  CAS  Google Scholar 

  • Brookes PC, McGrath SP, Heijnen C (1986) Metal residues in soils previously treated with sewage-sludge and their effects on growth and nitrogen fixation by blue-green algae. Soil Biol Biochem 18:345–353. doi:10.1016/0038-0717(86)90037-4

    Article  CAS  Google Scholar 

  • Brown GK, McCarthy P, Leenheer JA (1999) Simultaneous determination of Ca, Cu, Ni, Zn and Cd binding strength with fulvic acid fractions. Anal Chim Acta 402:169–181

    CAS  Google Scholar 

  • Bruins S, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Safe 45:198–207. doi:10.1006/eesa.1999.1860

    Article  CAS  Google Scholar 

  • Burkhardt EM, Bischoff S, Akob DM, Büchel G, Küsel K (2010) Heavy metal tolerance of Fe(III)-reducing microbial communities in a contaminated creek bank soil. Appl Environ Microbiol 77(9):3132–3136. doi:10.1128/AEM.02085-10

    Article  CAS  Google Scholar 

  • Burns RG (1978) Soil enzymes. Academic Press, London

    Google Scholar 

  • Caille N, Swanwick S, Zhao FJ, McGrath SP (2004) Arsenic hyperaccumulation by Pteris vittata from arsenic contaminated soils and the effect of liming and phosphate fertilization. Environ Pollut 132:113–120. doi:10.1016/j.envpol.2004.03.018

    Article  CAS  Google Scholar 

  • Cameron K, Beare M, Mclaren R, Hong D (1998) Selecting physical, chemical and biological indicators of soil quality for degraded or polluted soils. In: Symposium at the 16th world congress of soil science, Montpellier, France, paper no. 2516

  • Castaldi S, Rutigliano FA, Virzo De Santo A (2004) Suitability of soil microbial parameters as indicators of heavy metal pollution. Water Air Soil Pollut 158:21–35. doi:10.1023/B:WATE.0000044824.88079.d9

    Article  CAS  Google Scholar 

  • CEC: Commission of the European Communities (1986) Council Directives of 12 June 1986 on the protection of the environment, and in particular of the soils, when sewage sludge is used in agriculture. Off J Eur Commun L181(86/278/EEC):6–12

  • Chander K, Brookes PC (1991) Effects of heavy metals from past applications of sewage sludge on microbial biomass and organic matter accumulation in a sandy loam and a silty loam UK soil. Soil Biol Biochem 23:927–932. doi:10.1016/0038-0717(91)90172-G

    Article  Google Scholar 

  • Chandra SK, Kamala CT, Chary NS, Balaram V, Garcia G (2005) Potential of Hemidesmus indicus for phytoextraction of lead from industrially contaminated soils. Chemosphere 58:507–514. doi:10.1016/j.chemosphere.2004.09.022

    Article  CAS  Google Scholar 

  • Chang JS, Hwang YP, Fong YM, Lin PJ (1999) Detoxification of mercury by immobilized mercuric reductase. J Chem Technol Biotechnol 74:965–973. doi:10.1002/(SICI)1097-4660(199910)74:10<965:AID-JCTB135>3.0.CO;2-R

    Article  CAS  Google Scholar 

  • Chaudhary AM, McGrath SP (1996) Toxicity of organic compounds to the indigenous population of Rhizobium Leguminosarum biovar trifolii in soil. Soil Biol Biochem 28:1483–1487. doi:10.1016/S0038-0717(96)00156-3

    Article  Google Scholar 

  • Chaudri AM, McGrath SP, Giller KE, Angle JS, Chaney RL (1993) Screening of isolates and strains of Rhizobium leguminosarum biovar trifolii for heavy metal resistance using buffered media. Environ Toxicol Chem 12:1643–1651. doi:10.1002/etc.5620120913

    Article  CAS  Google Scholar 

  • Chen HM, Zheng CR, Tu C, Shen ZG (2000) Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere 41:229–234. doi:10.1016/S0045-6535(99)00415-4

    Article  CAS  Google Scholar 

  • Christensen TH (1984) Cadmium soil sorption at low concentration. I. Effect of time, cadmium load, pH and calcium. Water Air Soil Pollut 21:105–114. doi:10.1007/BF00163616

    Article  CAS  Google Scholar 

  • Collins YE, Stotzky G (1992) Heavy metals alter the electro-kinetic properties of bacteria, yeast and clay minerals. Appl Environ Microbiol 58:1592–1600

    CAS  Google Scholar 

  • Dahmani-Muller H, van Oort F, Gelie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109:231–238

    CAS  Google Scholar 

  • de Souza MP, Chu D, Zhao M, Zayed AM, Ruzin SE, Schichnes D, Terry N (1999) Rhizosphere bacteria enhance selenium accumulation and volatilization by Indian mustard. Plant Physiol 119:565–574

    Google Scholar 

  • Dias HE Jr, Moreira FMS, Siquera JO, Silva R (1998) Heavy metals, microbial density and activity in a soil contaminated with wastes from the zinc industry. Rev Bras Cienc Solo 22:631–640

    Google Scholar 

  • Dick RP (1997) Soil enzyme activities as integrative indicators of soil health. In: Pankhurst CE, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CAB, Wallingford, pp 121–156

    Google Scholar 

  • Dick RP, Breakwell DP, Turco RF (1996) Soil enzyme activities and biodiversity measurements as integrative microbiological indicators. In: Dick RP, Lal R, Lowery B, Rice CW, Stott DE (eds) Methods of assessing soil quality. SSSA Spec Publ No. 49, Madison, pp 247–271

    Google Scholar 

  • Dommergues YR, Diem HD, Ganry F (1980) The effect of soil microorganisms on plant productivity. Microbiologist. OSTROM/CNRS, Dakar, Senegal and CNRA/ISRA, Bambey, Senegal

  • Ebbs SD, Kochian LV (1998) Phytoextraction of zinc by oat (Avena sativa), barley (Hordeum vulgare), and Indian mustard (Brassica juncea). Environ Sci Technol 32:802–806

    CAS  Google Scholar 

  • Ebbs SD, Lasat MM, Brandy DJ, Cornish J, Gordon R, Kochian LV (1997) Phytoextraction of cadmium and zinc from a contaminated soil. J Environ Qual 26:1424–1430. doi:10.2134/jeq1997.00472425002600050032x

    Article  CAS  Google Scholar 

  • Eisler R (1988) Lead hazards to fish, wildlife and invertebrates: a synoptic review. Biological report 85 (1.14). United States Fish and Wildlife Service

  • Emmerling C, Schloter M, Hartmann A, Kandeler E (2002) Functional diversity of soil organisms, a review of recent research activities in Germany. J Plant Nutr Soil Sci 165:408–420. doi:10.1002/1522-2624(200208)165:4<408:AID-JPLN408>3.0.CO;2-3

    Article  CAS  Google Scholar 

  • Entry JA, Watrud LS, Reeves M (1999) Accumulation of 137Cs and 90Sr from contaminated soil by three grass species inoculated with mycorrhizal fungi. Environ Pollut 104:449–457. doi:10.1016/S0269-7491(98)00163-8

    Article  CAS  Google Scholar 

  • Feng D, Aldrich C (2004) Adsorption of heavy metals by biomaterials derived from the marine alga Ecklonia maxima. Hydrometallurgy 73:1–10. doi:10.1016/S0304-386X(03)00138-5

    Article  CAS  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    CAS  Google Scholar 

  • Filser J, Fromm H, Nagel RF, Winter K (1995) Effects of previously intensive agricultural management on microorganisms and biodiversity of soil fauna. Plant Soil 170:123–129. doi:10.1007/BF02183060

    Article  CAS  Google Scholar 

  • Fine P, Scagnossi A, Chen Y, Milgelgrin U (2005) Practical and mechanistic aspects of the removal of cadmium from aqueous systems using peat. Environ Pollut 138:358–367. doi:10.1016/j.envpol.2005.03.003

    Article  CAS  Google Scholar 

  • Francis AJ, Dodge CJ (1998) Remediation of soils and wastes contaminated with uranium and toxic metals. Environ Sci Technol 32:3933–3998

    Google Scholar 

  • Frattini CJ, Ledue LG, Ferroni GD (2000) Strain variability and effect of organic compounds on the growth of the chemolithotrophic bacteriumThiobacillus ferrooxidans. Antonie Van Leeuwenhoek 77:57–64

    CAS  Google Scholar 

  • Freedman B, Hutchinson TC (1980) Effects of smelter pollutants on forest leaf litter decomposition near a nickel copper smelter at Sudbury, Ontario. Can J Bot Q8:1722–1736. doi:10.1139/b80-200

    Article  Google Scholar 

  • 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. doi:10.1007/s0021663540750

    Article  CAS  Google Scholar 

  • Frostegard A, Tunlid A, Baath E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from 2 soil types experimentally exposed to different heavy-metals. Appl Environ Microbiol 59:3605–3617

    CAS  Google Scholar 

  • Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46:835–840. doi:10.1007/BF01935534

    Article  Google Scholar 

  • Gadd GM (1993) Microbial formation and transformation of organometallic and organometalloid compounds. FEMS Microbiol Rev 11:297–316. doi:10.1111/j.1574-6976.1993.tb00003.x

    Article  CAS  Google Scholar 

  • Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Environ Biotechnol 11:271–279. doi:10.1016/S0958-1669(00)00095-1

    Article  CAS  Google Scholar 

  • Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119. doi:10.1016/jgeoderma.2004.01.002

    Article  CAS  Google Scholar 

  • Gadd GM, Griffiths AJ (1978) Microorganisms and heavy metal toxicity. Microb Ecol 4:303–317. doi:10.1007/BF02013274

    Article  CAS  Google Scholar 

  • Gao Y, Zhou P, Mao L, Zhi Y, Shi W-J (2010) Assessment of effects of heavy metals combined pollution on soil enzyme activities and microbial community structure: modified ecological dose–response model and PCR-RAPD. Environ Earth Sci 60:603–612. doi:10.1007/s12665-009-0200-8

    Article  CAS  Google Scholar 

  • Gardea-Torresdey JL, Gonzalez JH, Tiemann KJ, Rodriguez O, Gamez G (1998) Phytofiltration of hazardous cadmium, chromium, lead and zinc ions by biomass of Medicago sativa (alfalfa). J Hazard Mater 57:29–39. doi:10.1016/S0304-3894(97)00072-1

    Article  CAS  Google Scholar 

  • Gharieb MM, Gadd GM (1998) Evidence for the involvement of vacuolar activity in metal(loid)s tolerance: vacuola-lacking and defective mutants ofSaccharomyces cerevisiae display higher sensitivity to chromate, telurite and selenite. Biometals 11:101–106. doi:10.1023/A:1009221810760

    Article  CAS  Google Scholar 

  • Gharieb MM, Kierans M, Gadd GM (1999) Transformation and tolerance of tellurite by filamentous fungi: accumulation, reduction and volatilization. Mycol Res 103:299–305. doi:10.1017/S0953756298007102

    Article  CAS  Google Scholar 

  • Giller KE, McGrath SP, Hirsch PR (1989) Absence of nitrogen fixation in clover grown in soil subject to long-term contamination with heavy metals is due to ineffective Rhizobium. Soil Biol Biochem 21:841–848. doi:10.1016/0038-0717(89)90179-X

    Article  CAS  Google Scholar 

  • Giller KE, Nitter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414. doi:10.1016/S0038-0717(97)00270-8

    Article  CAS  Google Scholar 

  • Giller KE, Witter E, McGrath SP (2009) Heavy metals and soil microbes. Soil Biol Biochem 41:2031–2037. doi:10.1016/j.soilbio.2009.04.026

    Article  CAS  Google Scholar 

  • Goel S, Malik JA, Nayyar H (2009) Molecular approach for phytoremediation of metal contaminated sites. Arch Agron Soil Sci 55:451–475. doi:10.1080/03650340902832861

    Article  CAS  Google Scholar 

  • Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122. doi:10.1007/s00425-006-0225-0

    Article  CAS  Google Scholar 

  • Gounou C, Bousserrhine N, Varrault G, Mouchel J-M (2010) Influence of the Iron-reducing bacteria on the release of heavy metals in anaerobic river sediment. Water Air Soil Pollut. doi:10.1007/s11270-010-0327-y

    Article  Google Scholar 

  • Gravot A, Lieutaud A, Verret F, Auroy P, Vavasseur A, Richaud P (2004) AtHMA3, a plant P1B-ATPase, functions as a Cd/Pb transporter in yeast. FEBS Lett 561:22–28. doi:10.1016/S0014-5793(04)00072-9

    Article  CAS  Google Scholar 

  • Groot JR, Houba VG (1995) A comparison of different indices of nitrogen mineralization. Biol Fertil Soils 19:1–9. doi:10.1007/BF00336338

    Article  CAS  Google Scholar 

  • Harrington JM, Fendorf SE, Rosenzweig RF (1998) Biotic generation of arsenic (III) in metal(loid)-contaminated freshwater lake sediments. Environ Sci Technol 32:2425–2430

    CAS  Google Scholar 

  • Harris PG (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

    Google Scholar 

  • Harris J (2009) Soil Microbial communities and restoration ecology: facilitators or followers? Science 325:573–574. doi:10.1126/science.1172975

    Article  CAS  Google Scholar 

  • Hassen A, Saidi N, Cherif M, Bondabous A (1998) Resistance of environmental bacteria in heavy metals. Bioresour Technol 64:7–15. doi:10.1016/S0960-8524(97)00161-2

    Article  CAS  Google Scholar 

  • Hayat S, Ahmad I, Azam ZM, Ahmad A, Inam A, Samullah A (2002) Effect of long-term application of oil refinery waste water on soil health. World J Microbiol Biotechnol 17:379–384. doi:10.1016/S0960-8524(02)00027-5

    Article  Google Scholar 

  • Hirayama T, Kieber JJ, Hirayama N, Kogan M, Guzman P, Nourizadeh S, Alonso JM, Dailey WP, Dancis A, Ecker JR (1999) Responsive-to-antagonist1, a Menkes/Wilson disease related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97:383–393. doi:10.1016/S0092-8674(00)80747-3

    Article  CAS  Google Scholar 

  • Hobman JL, Wilson JR, Brown NL (2000) Microbial mercury reduction. In: Lovley DR (ed) Environmental microbe–metal interactions. Am Soc Microbiol, Washington, pp 177–197

    Google Scholar 

  • Holmes D, Finneran K, O’Neil R, Lovley D (2002) Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer and sediments. Appl Environ Microbiol 68(5):2300–2306

    CAS  Google Scholar 

  • Hoppe S, Sundbum M, Borg H, Breitholtz M (2015) Prediction of Cu toxicity in three aquatic species using bioavailability tools in four Swedish soft freshwaters. Environ Sci Eur 27:25. doi:10.1186/s12302-015-0058-1

    Article  CAS  Google Scholar 

  • Horckmans L, Swennen R, Deckers J (2007) Retention and release of Zn and Cd in spodic horizons as determined by pHstat analysis and single extractions. Sci Total Environ 376:86–89. doi:10.1016/j.scitotenv.2007.01.077

    Article  CAS  Google Scholar 

  • Hund-Rinke K, Kordel W (2003) Underlying issues on bioassessibility and bioavailability: experimental methods. Ecotoxicol Environ Saf 56:52–62. doi:10.1016/S0147-6513(03)00050-2

    Article  CAS  Google Scholar 

  • Jarup L (2003) Hazards of heavy metal contamination. Br Med Bullet 68:167–182. doi:10.1093/bmb/ldg032

    Article  Google Scholar 

  • Kabata-Pendias A (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Kamaludeen SPB, Ramasamy K (2008) Rhizoremediation of metals: harnessing microbial communities. Indian J Microbiol 48:80–88. doi:10.1007/s12088-008-0008-3

    Article  CAS  Google Scholar 

  • Kandeler E, Kampichler C, Horak O (1996) Influence of heavy metals on functional diversity of soil microbial communities. Biol Fertil Soils 23:299–306. doi:10.1007/BF00335958

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/s003740000268

    CAS  Google Scholar 

  • Kara Ö, Bolat I, Çakıroğlu K, Öztürk M (2008) Plant canopy effects on litter accumulation and soil microbial biomass in two temperate forests. Biol Fertil Soils 45:193–198. doi:10.1007/s00374-008-0327-x

    Article  Google Scholar 

  • Kemner KM, Kelly SD, Lai B, Maser J, O’Loughlin EJ, Sholto-Douglas D, Cai Z, Schneegurt MA, Kulpa-Jr CF, Nealson KH (2004) Elemental and redox analysis of single bacterial cells by X-ray microbeam analysis. Sci Mag 306(5696):686–687. doi:10.1126/science.1103524

    Article  CAS  Google Scholar 

  • Khan MS, Zaidi A, Wani PA, Oves M (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7:1–19. doi:10.1007/s10311-008-0155-0

    Article  CAS  Google Scholar 

  • Kirkham MB (2006) Cadmium in plants and polluted soils: effects of soil factors, hyperaccumulation and amendments. Geoderma 137:19–32. doi:10.1016/j.geoderma.2006.08.024

    Article  CAS  Google Scholar 

  • Kizilkaya R, Aşkin T, Bayrakli B, Sağlam M (2004) Microbiological characteristics of soils contaminated with heavy metals. Eur J Soil Biol 40:95–102. doi:10.1016/j.ejsobi.2004.10.002

    Article  CAS  Google Scholar 

  • Knight BP, 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

    CAS  Google Scholar 

  • Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238. doi:10.1021/es00005a014

    Article  CAS  Google Scholar 

  • Kuperman RG, Carreiro MM (1997) Soils heavy metal concentration, microbial biomass and enzyme activities in a contaminated grassland ecosystem. Soil Biol Biochem 29:179–190. doi:10.1016/S0038-0717(96)00297-0

    Article  CAS  Google Scholar 

  • Lăcătuşu R, Rauta C, Carstea S, Ghelase I (1996) Soil–plant–man relationships in heavy metal polluted area in Romania. Appl Geochem 11:105–107. doi:10.1016/0883-2927(95)00101-8

    Article  Google Scholar 

  • Lavelle P, Brussards L, Hendrix P (1999) Earthworm management in tropical agroecosystems. CABI, Wallingford

    Google Scholar 

  • Leita L, De Nobili 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. doi:10.1007/BF00336144

    Article  CAS  Google Scholar 

  • Linton PE, Shotbolt L, Thomas AD (2007) Microbial communities in long-term heavy metal contaminated ombrotrophic peats. Water Air Soil Pollut 186:97–113. doi:10.1007/s11270-007-9468-z

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Lloyd JR, Sole VA, Van Praagh CVG, Lovley DR (2000) Direct and Fe(II)-mediated reduction of technetium by Fe(III)-reducing bacteria. Appl Environ Microbiol 66(9):3743–3749. doi:10.1128/AEM.66.9.3743-3749.2000

    Article  CAS  Google Scholar 

  • Lock K, Janssen CR (2003) Influence of aging on metal availability in soils. Rev Environ Contamin Toxicol 178:1–21. doi:10.1007/0-387-21728-2_1

    Article  CAS  Google Scholar 

  • Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2001) Phytoremediation of heavy metal-contaminated soils. J Environ Qual 30:1919–1926. doi:10.2134/jeq2001.1919

    Article  CAS  Google Scholar 

  • Lovley DR, (2000) Fe(III) and Mn(IV) reduction. In: Lovley DR (ed) Environmental microbe–metal interactions. Am Soc Microbiol, Washington, pp 3–30

  • Ma LQ, Komar KM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579. doi:10.1038/35054664

    Article  CAS  Google Scholar 

  • Macaskie LE, Dean ACR (1989) Microbial metabolism, desolubilization and deposition of heavy metals: uptake by immobilized cells and application to the treatment of liquid wastes. In: Mizrahi A (ed) Biological waste treatment. Alan R. Liss, New York, pp 150–201

    Google Scholar 

  • Madejon P, Murillo JM, Maranon T, Cabrera F, Lopez R (2002) Bioaccumulation of As, Cd, Cu, Fe and Lead in wild grasses affected by the Aznalcollar mine spill (SW Spain). Sci Total Environ 290:105–120

    CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (lycopersicon esculentum L.). Chemosphere 69:220–228. doi:10.1016/j.chemosphere.2007.04.017

    Article  CAS  Google Scholar 

  • Mary B, Recous S, Darwis D, Robins D (1996) Interactions between decomposition of plant residues and nitrogen cycling in soil. Plant Soil 181:71–82. doi:10.1007/BF00011294

    Article  CAS  Google Scholar 

  • McGrath SP, Brookes PC, Giller KE (1988) Effects of potentially toxic metals in soil derived from past applications of sewage sludge on nitrogen fixation by Trifolium repens L. Soil Biol Biochem 20:415–424. doi:10.1016/0038-0717(88)90052-1

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ, Lombi E (2002) Phytoremediation of metals, metalloids, and radionuclides. Adv Agron 75:1–56. doi:10.1016/S0065-2113(02)75002-5

    Article  CAS  Google Scholar 

  • Megharaj KVM, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135. doi:10.1016/S1093-0191(02)00135-1

    Article  CAS  Google Scholar 

  • Mehmood T, Akbar Malik S, Hussain ST (2009) Roles of microbes in nitrogen and metal hyperaccumulation by toxilaion Eichhornia crassipes. Afr J Microbiol Res 3(12):914–924

    CAS  Google Scholar 

  • Méndez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments—an emerging remediation technology. Environ Health Perspect 116(3):278–283. doi:10.1289/ehp.10608

    Article  CAS  Google Scholar 

  • Misra V, Tiwari A, Shukla B, Seth CS (2009) Effects of soil amendments on the bioavailability of heavy metals from zinc mine tailings. Environ Monitor Assess 155:467–475. doi:10.1007/s10661-008-0449-5

    Article  CAS  Google Scholar 

  • Morales-Barrera L, Cristiani-Urbina E (2008) Hexavalent chromium removal by a Trichoderma inhamatum fungal strain isolated from tannery effluent. Water Air Soil Pollut 187:327–336. doi:10.1007/s11270-007-9520-z

    Article  CAS  Google Scholar 

  • Moreno JL, Hernàndez T, García C (1999) Effects of a cadmium contaminated sewage sludge compost on dynamics of organic matter and microbial activity in an arid soil. Biol Fertil Soils 28:230–237. doi:10.1007/s003740050487

    Article  CAS  Google Scholar 

  • Moreno JL, Landi C, García L, Falchini L, Pietramellara G, Nannipieri P (2001) The ecological dose value (ED50) for assessing Cd toxicity on ATP content and dehydrogenase and urease activities of soil. Soil Biol Biochem 33:483–489. doi:10.1016/S0038-0717(00)00189-9

    Article  CAS  Google Scholar 

  • Moreno JL, García C, Hernàndez T (2003) Toxic effect of cadmium and nickel on soil enzymes and the influence of adding sewage sludge. Eur J Soil Sci 54:377–386. doi:10.1046/j.1365-2389.2003.00533.x

    Article  CAS  Google Scholar 

  • Mudgal V, Madaan N, Mudgal A (2010) Heavy metals in plants: phytoremediation: plants used to remediate heavy metal pollution. Agric Biol J North Am 1:40–46.

  • Muhlbachova G, Simon T (2003) Effects of zeolite amendment on microbial biomass and respiratory activity in heavy metals contaminated soil. Plant Soil Environ 49:536–541

    CAS  Google Scholar 

  • Muhulbachova G, Tlustos P (2006) Effects of liming on the microbial biomass and its activities in soil long-term contaminated by toxic metals. Plant Soil Environ Manag 9:115–121

    Google Scholar 

  • Naees M, Ali Q, Shahbaz M, Ali F (2011) Roles of rhizobacteria in phytoremediation of heavy metals: an overview. Int Res J Plant Sci 2(8):220–232

    Google Scholar 

  • Naidu R, Kookana RS, Sumner ME, Harter RD, Tiller KG (1997) Cadmium sorption and transport in variable charged soils: a review. J Environ Qual 26:602–617. doi:10.2134/jeq1997.00472425002600030004x

    Article  CAS  Google Scholar 

  • Naidu R, Oliver D, McConnell S (2003) Heavy metal phytotoxicity in soils. In: Proceedings of the fifth national workshop on the assessment of site contamination. National Environmental Protection Council, Australia, pp 235–241

  • Naidu R, Rogers S, Gupta VVSR, Kookana RS, Bolan NS, Andriano D (2006) Bioavailability of heavy metals in the soil-plant environment and its potential role in risk assessment an over view. In: 4th International conference on the biogeochemistry of trace elements, pp 757–758

  • Novarro-Noya YE, Jan-Roblero J, Gonzàlez-Chàvez MDC, Hernàndez-Gama R, Hernàndez-Rodríguez C (2010) Bacterial communities associated with the rhizosphere of pioneer plants (Bahia xylopoda and Viguiera linearis). Antonie Van Leeuwenhoek 97:335–349. doi:10.1007/s10482-010-9413-9

    Article  CAS  Google Scholar 

  • Nriagu JO (1990) The rise and fall of leaded gasoline. Sci Total Environ 92:13–28. doi:10.1016/0048-9697(90)90318-O

    Article  CAS  Google Scholar 

  • Olsen BH, Thornton I (1982) The resistance pattern to metals of bacterial population in contaminated land. Eur J Soil Sci 33:271–277. doi:10.1111/j.1365-2389.1982.tb01765.x

    Article  Google Scholar 

  • Oremland RS, Steinberg NA, Presser TS, Miller LG (1991) In situ bacterial selenate reduction in the agricultural drainage systems of Western Nevada. Appl Environ Microbiol 57:615–617

    CAS  Google Scholar 

  • Osborn D, Eney WJ, Bull KR (1983) The toxicity of trialkyl lead compounds to lead. Environ Pollut 31:261–275. doi:10.1016/0143-1471(83)90063-6

    Article  CAS  Google Scholar 

  • Pajuelo E, Rodríguez-Llorente ID, Lafuente A, Caviedes MA (2011) Legume-Rhizobium symbioses as a tool for bioremediation of heavy metal polluted soils. In: Khan MS, Zaidi A, Goel R, Musarrat J (eds) Biomanagement of metal-contaminated soils. Environmental pollution, vol 20. Springer, New York, pp 95–124. doi:10.1007/978-94-007-1914-9_4

    Chapter  Google Scholar 

  • Pankhurst CE, Hawke BG, McDonald HJ, Kirkby CA, Buckerfield JC, Michelsen P, O’Brien KA, Gupta VVSR, Doube BM (1995) Evaluation of soil biological properties as potential bioindicators of soil health. Anim Prod Sci 35:1015–1028. doi:10.1071/EA9951015

    Article  Google Scholar 

  • Pathak A, Dastidar MG, Sreskrishan TR (2009) Review bioleaching of heavy metals from sewage sludge: a review. J Environ Manag 90:2343–2353. doi:10.1016/j.jenvman.2008.11.005

    Article  CAS  Google Scholar 

  • Pelczar MJ Jr, Chen ECS, Krleg NR (1986) Microbiology, 5th edn. McGraw Hill, New York

    Google Scholar 

  • Phillips EJP, Landa ER, Lovley DR (1995) Remediation of uranium contaminated soils with bicarbonate extraction and microbial U(VI) reduction. J Ind Microbiol 14:203–207. doi:10.1007/BF01569928

    Article  CAS  Google Scholar 

  • Pipe AE (1992) Pesticide effect on soil algae and cynobacteria. Rev Environ Contam Toxicol 127:95–170. doi:10.1007/978-1-4613-9751-9_4

    Article  CAS  Google Scholar 

  • Pishchik VN, Provorov NA, Vorobyov NI, Chizevskaya EP, Safronova VI, Tuev AN, Kozhemyakov AP (2009) Interactions between plants and associated bacteria in soils contaminated with heavy metals. Microbiology 78:785–793. doi:10.1134/S0026261709060162

    Article  CAS  Google Scholar 

  • Pongratz R, Heumann KG (1999) Production of methylated mercury, lead and cadmium by marine bacteria as a significant natural source for atmospheric heavy metals in Polar Regions. Chemosphere 39:89–102. doi:10.1016/S0045-6535(98)00591-8

    Article  CAS  Google Scholar 

  • Prasad NMV, Freitas HMD (2003) Metal hyperaccumulation in plants—biodiversity prospecting for phytoremediation technology. Electr J Biotechnol 6:286–321. http://www.ejbiotechnology.info/content/vol6/issue3/full/6

  • Rajaniemi TK, Allison VJ (2009) Abiotic conditions and plant cover differentially affect microbial biomass and community composition on dune gradients. Soil Biol Biochem 41:102–109. doi:10.1016/j.soilbio.2008.10.001

    Article  CAS  Google Scholar 

  • Rama Rao VS, Wilson CH, Maruthi Mohan P (1997) Zinc resistance inNeurospora crassa. Biometals 10:147–156. doi:10.1023/A:1018339425355

    Article  Google Scholar 

  • Rasmussen LD, Sorensen SJ (2001) Effects of mercury contamination on the culturable heterotrophic, functional and genetic diversity of the bacterial community in soil. FEMS Microbiol Ecol 36:1–9

    CAS  Google Scholar 

  • Rathnayake VN, Megharaj M, Bolan N, Naidu R (2010) Tolerance of heavy metals to gram positive soil bacteria. Int J Civ Environ Eng 2(4):191–195

    Google Scholar 

  • Rattan RK, Datta SP, Chandra S, Saharan N (2002) Heavy metals and environmental quality: Indian scenario. Fertil News 47(11):21–40

    CAS  Google Scholar 

  • Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean-up the environment. Wiley, New York, pp 193–230

    Google Scholar 

  • Rehman A, Anjum MS (2010) Cadmium Uptake by Yeast, Candida tropicalis, isolated from industrial effluents and its potential use in wastewater clean-up operations. Water Air Soil Pollut 205:149–159. doi:10.1007/s11270-009-0062-4

    Article  CAS  Google Scholar 

  • Rehman A, Farooq H, Shakoori AR (2007) Copper tolerant yeast, Candida tropicalis, isolated from industrial effluents: its potential use in wastewater treatment. Pak J Zool 39:405–412

    CAS  Google Scholar 

  • Renella G, Ortigoza ALR, Landi L, Nannipieri P (2003) Additive effects of copper and zinc on cadmium toxicity on phosphatase activities and ATP content of soil as estimated by the ecological dose (ED50). Soil Biol Biochem 35:1203–1210. doi:10.1016/S0038-0717(03)00181-0

    Article  CAS  Google Scholar 

  • Ribeiro AR, Umbuzeiro GD (2014) Effects of a textile azo dye on mortality, regeneration, and productive performance of the planarian, Girardia tigrina. Environ Sci Eur 26:22. http://www.enveurope.com/content/26/1/22

  • Roane TM, Pepper IL (1989) Microbial responses to environmentally toxic cadmium. Microbial Ecol 38:358–364. doi:10.1007/s002489901001

    Article  Google Scholar 

  • Rosen BP (2002) Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol Part A Mol Integr Physiol 133:689–693. doi:10.1016/S1095-6433(02)00201-5

    Article  Google Scholar 

  • Salazar MJ, Rodriguez JH, Cid CV, Bernardelli CE, Donati ER, Pignata ML (2016) Soil variables that determines lead accumulation in Bidens pilosa L. and Tagetes minuta L. growing on polluted soils. Geoderma 279:97–108. doi:10.1016/j.geoderma.2016.06.011

    Article  CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley D, Chet I, Raskin I (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Nat Biotechnol 13:468–474. doi:10.1038/nbt0595-468

    Article  CAS  Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668. doi:10.1146/annurev.arplant.49.1.643

    Article  CAS  Google Scholar 

  • Schuller E (1989) Enzyme activities and microbial biomass in old landfill soils with long-term metal pollution. Verh Ges Okol 18:339–348

    Google Scholar 

  • Sekhar KC, Kamala CT, Chary NS, Sastry ARK, Rao TN, Vairamani M (2004) Removal of lead from aqueous solutions using an immobilized biomaterial derived from a plant biomass. J Hazard Mater 108:111–117. doi:10.1016/j.jhazmat.2004.01.013

    Article  CAS  Google Scholar 

  • Shakoori AR, Qureshi F (2000) Cadmium resistant bacteria from industrial effluents and their role in environmental clean-up. Pak J Zool 32:165–178

    CAS  Google Scholar 

  • Shakoori AR, Rehman A, Haq RU (2004) Multiple metal resistance in the ciliate protozoan, Vorticella microstoma, isolated from industrial effluents and its potential in bioremediation of toxic wastes. Bull Environ Contamin Toxicol 72:1046–1051. doi:10.1007/s00128-004-0349-5

    Article  CAS  Google Scholar 

  • Sheng PX, Ting Y-P, Chen JP, Hong L (2004) Sorption of lead, copper, cadmium, zinc, and nickel by marine algal biomass: characterization of biosorptive capacity and investigation of mechanisms. J Coll Interf Sci 275:131–141. doi:10.1016/j.jcis.2004.01.036

    Article  CAS  Google Scholar 

  • Shuman LM (1985) Fractionation method for soil microelements. Soil Sci 140:11–22. OSTI ID: 6337444

    CAS  Google Scholar 

  • Silver S, Phung LT (2005) A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotech 32:587–605. doi:10.1007/s10295-005-0019-6

    Article  CAS  Google Scholar 

  • Simmonds MA (1979) Tertiary treatment with aquatic macrophytes. Prog Water Technol 11:507–518

    CAS  Google Scholar 

  • Simona C, Angela RF, Santo Amalia VD (2004) Suitability of soil microbial parameters as indicators of heavy metal pollution. Water Air Soil Pollut 158(1):21–35. doi:10.1023/B:WATE.0000044824.88079.d9

    Article  Google Scholar 

  • Smejkalova M, Mikanova O, Boruvka L (2003) Effects of heavy metals concentrations on biological activity of soil micro-organisms. Plant Soil Environ 49:321–326

    CAS  Google Scholar 

  • Smith SR (1991) Effects of sewage sludge application on soil microbial processes and soil fertility. Adv Soil Sci 16:191–212. doi:10.1007/978-1-4612-3144-8_4

    Article  Google Scholar 

  • Smith WL, Gadd GM (2000) Reduction and precipitation of chromate by mixed culture sulphate-reducing bacterial biofilms. J Appl Microbiol 88:983–991. doi:10.1046/j.1365-2672.2000.01066.x

    Article  CAS  Google Scholar 

  • Spain A, Alm D (2003) Implications of microbial heavy metal tolerance in the environment. Rev Undergrad Res 2:1–6

    Google Scholar 

  • Sparling GP (1992) Ratio of microbial biomass carbon as a scientific indicator of changes in soil organic matter. Aust J Soil Res 30:195–207. doi:10.1071/SR9920195

    Article  CAS  Google Scholar 

  • Sposito G (2008) The chemistry of soils, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Strojan CL (1978) Forest leaf litter decomposition in the vicinity of a zinc smelter. Oecologia 32:203–212. doi:10.1007/BF00366072

    Article  Google Scholar 

  • Subhani A, Changyong H, Zhengmiao X, Min L, Elghawry AM (2001) Impact of soil environment and agricultural practices on microbial/dehydrogenase enzyme activity in soil: a review. Pak J Biol Sci 4:333–338

    Google Scholar 

  • Swift MJ, Bignell DE, Moreira FMS, Huising EJ (2008) The inventory of soil biological diversity: concepts and General guidelines. In: Fatima MS, Moreira E, Jeroen H, David EB (eds) A handbook of tropical soil biology: sampling and characterization of below-ground biodiversity. Earthscan Publishers, New York

    Google Scholar 

  • Tack FMG, Van Ranst E, Lievens C, Vandenberghe RE (2006) Soil solution Cd, Cu and Zn concentrations as affected by short-time drying or wetting: the role of hydrous oxides of Fe and Mn. Geoderma 137:83–87. doi:10.1016/j.geoderma.2006.07.003

    Article  CAS  Google Scholar 

  • Tarradelas J, Bitton G, Rossel D (2005) Soil ecotoxicology. CRC Press, Boca Raton

    Google Scholar 

  • Thomine S, Wang R, Ward JM, Crawford NM, Schroeder JI (2000) Cadmium and iron transport by members of a plant metal transporter family inArabidopsis with homology to Nramp genes. Proc Natl Acad Sci USA 97:4991–4996

    CAS  Google Scholar 

  • Timothy AA, David M, Linda M, Annette P, Eric D, Chris T, Kristin C (1999) Baseline human and ecological risk assessment. Lower Fox River Wisconsin. Wisconsin Department of Natural Resources, Madison

    Google Scholar 

  • Trevors JT, Stratton GW, Gadd GM (1986) Cadmium transport, resistance, and toxicity in bacteria, algae, and fungi. Can J Microbiol 32:447–464. doi:10.1139/m86-085

    Article  CAS  Google Scholar 

  • Türkdoğan MK, Kilicel F, Kara K, Tuncer I, Uygan I (2003) Heavy metals in soil, vegetables and fruits in the endemic upper gastrointestinal cancer region of Turkey. Environ Toxicol Pharmacol 13:175–179. doi:10.1016/S1382-6689(02)00156-4

    Article  CAS  Google Scholar 

  • Turpeinen R (2002) Interactions between metals, microbes and plants—bioremediation of arsenic and lead contaminated soils. PhD dissertation, Department of Ecological and Environmental Science, University of Helsinki

  • Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135. doi:10.1016/S1093-0191(02)00135-1

    Article  CAS  Google Scholar 

  • Wang Y, Shi J, Wang H, Lin Q, Chen X (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicol Environ Saf 67:75–81. doi:10.1016/j.ecoenv.2006.03.007

    Article  CAS  Google Scholar 

  • Wang J, Zhang CB, Jin ZX (2009) The distribution and phytoavailability of heavy metal fractions in rhizosphere soils of Paulowniu fortunei (seem) Hems near a Pb/Zn smelter in Guangdong, PR China. Geoderma 148:299–306. doi:10.1016/j.geoderma.2008.10.015

    Article  CAS  Google Scholar 

  • Wang Y, Zhan M, Zhu H, Guo S, Wang W, Xue B (2011) Distribution and accumulation of metals in soils and plant from a lead–zinc mineland in Guangxi, South China. Bull Environ Contam Toxicol. doi:10.1007/s00128-011-0473-y

    Article  Google Scholar 

  • Watanabe ME (1997) Phytoremediation on the brink of commercialization. Environ Sci Technol 31:182–186

    Google Scholar 

  • Weigand S, Anerwld K, Beck T (1995) Microbial biomass in agricultural top soils after 6 years bare fallow. Biol Fertil Soils 19:129–134. doi:10.1007/BF00336148

    Article  Google Scholar 

  • Windham L, Weis JS, Weis P (2001) Lead uptake, distribution, and effects in two dominant salt marsh macrophytes, Spartina alterniflora (Cordgrass) and Phragmites australis (Common Reed). Mar Pollut Bull 42(10):811–816. doi:10.1016/S0025-326X(00)00224-1

    Article  CAS  Google Scholar 

  • Witter E, Dahlin S (1995) Microbial utilization of [U-14C]-labeled straw and [U-13C]-labeled glucose in soils of contrasting pH and metal status. Soil Biol Biochem 27:1507–1516. doi:10.1016/0038-0717(95)00107-P

    Article  CAS  Google Scholar 

  • Wu T, Chellemi DO, Graham JH, Martin KJ, Rosskopf EN (2008) Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb Ecol 55:293–310. doi:10.1007/s00248-007-9276-4

    Article  Google Scholar 

  • Wyszkowska M, Wyszkowski M (2002) Effect of cadmium and magnesium on microbiological activity in soil. Pol J Environ Stud 11:585–591

    CAS  Google Scholar 

  • Xue SG, Chen YX, Reeves RD, Baker AJ, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ Pollut 131:393–399. doi:10.1016/j.envpol.2004.03.011

    Article  CAS  Google Scholar 

  • Yang Z, Liu S, Zheng D, Feng S (2006) Effects of cadmium, zinc and lead on soil enzyme activities. J Environ Sci 18:1135–1141. doi:10.1016/S1001-0742(06)60051-X

    Article  Google Scholar 

  • Yang R, Tang J, Chen X, Hu S (2007) Effects of coexisting plant species on soil microbes and soil enzymes in metal lead contaminated soils. Appl Soil Ecol 37:240–246. doi:10.1016/j.apsoil.2007.07.004

    Article  Google Scholar 

  • Yao H, Xu J, Huang C (2003) Substrate utilization pattern, biomass and activity of microbial communities in a sequence of heavy metal-polluted paddy soils. Geoderma 115:139–148. doi:10.1016/S0016-7061(03)00083-1

    Article  CAS  Google Scholar 

  • Yeung AT, Hsu C-N (2005) Electrokinetic remediation of cadmium contaminated clay. J Environ Eng 131:298–304. doi:10.1061/(ASCE)0733-9372(2005)131:2(298)

    Article  CAS  Google Scholar 

  • Zaguralskaya LM (1997) Microbiological monitoring of forest ecosystems in the northern taiga subzone in conditions of anthropogenic impact. Lesovedenie 5:3–12

    Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997. doi:10.1016/j.chemosphere.2005.12.057

    Article  CAS  Google Scholar 

  • Zhao FJ, Dunham SJ, McGrath SP (2002) Arsenic hyperaccumulation by different fern species. New Phytol 15:27–31. doi:10.1046/j.1469-8137.2002.00493.x

    Article  Google Scholar 

  • Zhou JM, Dang Z, Cai M, Liu CQ (2007) Soil heavy metal pollution around the Dabaoshan Mine, Guangdong Province, China. Pedosphere 17:588–594. doi:10.1016/S1002-0160(07)60069-1

    Article  CAS  Google Scholar 

  • Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413. doi:10.1016/j.envint.2006.12.005

    Article  Google Scholar 

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  1. Department of Soil Science, Faculty of Agriculture/Institute for Agricultural Research, Ahmadu Bello University, P.M.B. 1044, Samaru, Zaria, Nigeria

    Nafiu Abdu, Aliyu A. Abdullahi & Aisha Abdulkadir

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Abdu, N., Abdullahi, A.A. & Abdulkadir, A. Heavy metals and soil microbes. Environ Chem Lett 15, 65–84 (2017). https://doi.org/10.1007/s10311-016-0587-x

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