Skip to main content

Tolerance of Microorganisms in Soil Contaminated with Trace Metals: An Overview

  • Chapter
  • First Online:
Recent advances in Applied Microbiology

Abstract

Trace metal (TM) pollution of soil is a worldwide problem threatening the quality of human life and a proper environment. We investigated fungal and bacterial diversity of trace metal-polluted site contaminated with paper mill effluent in India. Twelve fungal dominant isolates, viz. Aspergillus, Penicillium, Fusarium, Cunninghamella, Simplicillium, Trichoderma, Rhizomucor, Cladosporium and Hypocrea, were identified. Subsequent screening approach to assess their TM tolerance was performed in vitro cultures which revealed that the majority of the isolates were tolerant to Ni-, Cu-, Zn- and Cd-amended medium. The minimum inhibitory concentration (MIC) for Ni, Cu, Zn and Cd was also determined in isolated strains of Aspergillus, Penicillium, Rhizomucor, Trichoderma and Fusarium to study the concentration of growth against various trace metals. A total of 22 bacterial isolates was also isolated using 16S rRNA, and the dominant genera such as Bacillus, Rhizobium, Microbacterium, Arthrobacter, Kribbella and Chitinophaga were identified. The relative growth and LD−50 were also estimated against the different trace metals from concentration 0.1 to 4 mM. Thus, these fungal and bacterial isolates showed a high TM tolerance and would be a great interest for their use in bioremediation to clean up TM-polluted soil.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

References

  • Aafi NE, Brhada F, Dary M, Maltouf AF, Pajuelo E (2012) Rhizostabilization of metals in soils using Lupinus luteus inoculated with the metal resistant rhizobacterium Serratia sp. MSMC 541. Int J Phytoremediation 14:261–274. doi:10.1080/15226514.2011.604693

    Article  CAS  PubMed  Google Scholar 

  • Abdelatey LM, Khalil WKB, Ali TH, Mahrous KF (2011) Heavy metal resistance and gene expression analysis of metal resistance genes in Gram-positive and Gram-negative bacteria present in Egyptian soils. J Appl Sci Env San 6:201–211

    CAS  Google Scholar 

  • Abou-Shanab RAI, Van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367. doi:10.1016/j.chemosphere.2006.12.051

    Article  CAS  PubMed  Google Scholar 

  • Adel Al-Gheethi AS, Noril I, Lalung J, Azan AM, Nurfarehah ZA, Kadir AB (2014) Biosorption of heavy metals and cephalexin from secondary effluents by tolerant bacteria. Clean Technol Envir 16(1):137–148

    Article  Google Scholar 

  • Adesoji AT, Ogunjobi AA, Olatoye IO, Douglas DR (2015) Prevalence of tetracycline resistance genes among multi-drug resistant bacteria from selected water distribution systems in southwestern Nigeria. Ann Clin Microbiol Antimicrob 14:35. doi:10.1186/s12941-015-0093-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmed I, Hayat S, Ahmed A, Samiullah IA (2001) Metal and antibiotic resistance traits in Bradyrhizobium sp (cajanus) isolated from soil receiving oil refinery wastewater. World J Microbiol Biotechnol 17:379–384

    Article  Google Scholar 

  • Akhtar S, Mahmood-ul-Hassan M, Ahmad R, Suthor V, Yasin M (2013) Metal tolerance potential of filamentous fungi isolated from soils irrigated with untreated municipal effluent. Soil Environ 32:55–62

    CAS  Google Scholar 

  • Akponah E (2013) Bacterial and fungal biosorbents of heavy metals associated with hydrocarbon contaminated rainforest soils of the Niger delta region of Nigeria. Eur J Exp Biol 3(3):95–100

    CAS  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of metals-concepts and applications. Chemosphere 91:869–881. doi:10.1016/j.chemosphere.2013.01.075

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Meyer EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  • Anahid S, Yaghmaei S, Ghobadinejad Z (2011) Heavy metal tolerance of fungi. Scientia Iranica 18(3):502–508

    Article  CAS  Google Scholar 

  • Anderson DI, Hughes D (2014) Microbiological effects of sublethal levels of antibiotics. Nature Rev Microbiol 12:465–478. doi:10.1038/nrmicro3270

    Article  CAS  Google Scholar 

  • Andrew B, Brown M, Steven DS, Peter HT (2013) Microbial community responses to anthropogenically induced environmental change: towards a systems approach. Ecol Lett 16(Supplement S1):128–139. doi:10.1111/ele.12109

    Article  Google Scholar 

  • Anyanwu CU, Nwankwo SC, Moneke AN (2011) Soil bacterial response to introduced metal stress. Int J Basic Appl Sci 11(1):109–115

    Google Scholar 

  • Appenroth, K-J (2010) Defination of heavy metals and their role in biological systems. In: Sheramati I, Varma A (eds) Soil heavy metals. Soil biology, vol 19. Springer, Berlin, pp 19–29

    Google Scholar 

  • Bafana A, Krishnamurthi K, Patil M, Chakrabarti T (2010) Heavy metal resistance in Arthrobacter ramosus strain G2 isolated from mercuric salt-contaminated soil. J Hazard Mater 177(1–3):481–486. doi:10.1016/j.saa.2009.12.058

    Article  CAS  PubMed  Google Scholar 

  • Bargagli R (2000) Trace metals in Antarctica related to climate change and increasing human impact. Rev Environ Contam Toxicol 166:129–173

    CAS  PubMed  Google Scholar 

  • Bauer AW, Kirby WMM, Sherris JC (1996) Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 45(4):493–496

    Google Scholar 

  • Bello OA, Abdullahi OA (2016) Tolerance to heavy metals by some fungal isolates from petroleum refinery effluent in Kaduna, Nigeria. Br Microbiol Res J 12(6):1–8. doi:10.9734/BMRJ/2016/22728

    Article  Google Scholar 

  • Borjesson G, Menichetti L, Kirchmann H, Kätterer T (2012) Soil microbial community structure affected by 53 years of nitrogen fertilization and different organic amendments. Biol Fert Soils 48(3):245–257

    Article  Google Scholar 

  • Braud A, Jézéquel K, Bazot S, Lebeau T (2010) Enhanced phytoextraction of an agricultural Cr, hg and Pbcontaminated soil by bioaugmentation with siderophore producing bacteria. Chemosphere 74:280–286. doi:10.1016/j.chemosphere.2008.09.013

    Article  CAS  Google Scholar 

  • Brown SD, Palumbo AV, Panikov N, Ariyawansa T, Klingeman DM, Johnson KM, Land ML, Utturkar SM, Epstein SL (2012) Draft genome sequence for Microbacterium laevaniformans strain OR221, a bacterium tolerant to metals, nitrate, and low pH. J Bacteriol 194(12):3279–3280. doi:10.1128/JB.00474-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burford EP, Fomina M, Gadd GM (2003) Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineral Mag 67:1127–1155. doi:10.1180/0026461036760154

    Article  CAS  Google Scholar 

  • Carlsohn MR, Groth I, Spror C, Schutze B, Saluz HP, Munder T, Stackebrandt E (2007) Kribbella aluminosa sp. nov., isolated from a medieval alum slate mine. Int J Syst Evol Microbiol 57:1943–1947

    Article  CAS  Google Scholar 

  • Carson JK, Gonzalez-Quinones V, Murphy DV, Hinz C, Shaw JA, Gleeson DB (2010) Low poreconnectivity increases bacterial diversity in soil. Appl Environ Microbiol 76:3936–3942. https://doi.org/10.1128/AEM.03085-09

    Article  CAS  Google Scholar 

  • Cervantes C, Gutierrez-Corona F (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–137. doi:10.1111/j.1574- 6976.1994.tb00083.x

    Article  CAS  PubMed  Google Scholar 

  • Cetin SC, Karaca A, Kizilkaya R, Turgay OC (2012) Role of plant growth promoting bacteria and fungi in heavy metal detoxification. In: Sheramati VA (ed) Detoxification of heavy metals. Soil Biology, vol 30. Springer-Verlag, Berlin, pp 369–388

    Chapter  Google Scholar 

  • Chen J, Chen HM, Zhang YQ, Wei YZ, Li QP, Liu HY, Jing S, Zhang YQ, Yu LY (2011) Agromyces flavus sp. nov., an actinomycete isolated from soil. Int J Syst Evol Microbiol 61:1705–1709. doi:10.1099/ijs.0.023242-0

    Article  CAS  PubMed  Google Scholar 

  • Chen J, He F, Zhang X, Sun X, Zheng J, Zheng J (2014) Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiol Ecol 87:164–181. https://doi.org/10.1111/1574-6941.12212

    Article  Google Scholar 

  • Clara U, Filomena DL, Schumann P (2008) Kribbella catacumbae sp. nov. and Kribbella sancticallisti sp. nov., isolated from whitish-grey patinas in the catacombs of St Callistus in Rome, Italy. Int J Syst Evol Microbiol 58:2090–2097. doi:10.1099/ijs.0.65613-0

    Article  CAS  Google Scholar 

  • de Lima AF, de Moura GF, de Lima MA, de Souza PM, da sliva CA, De Campos GM, Do Nascimento AE (2011) Role of the morphology and polyphosphate in Trichoderma harzianum related to cadmium removal. Molecules 16(3):2486–2500. doi:10.3390/molecules16032486

    Article  CAS  PubMed  Google Scholar 

  • de Lima MAB, de Franco, Luciana O, de Souza, Patrícia M, do Nascimento, Aline E, da Silva, Carlos AA, de Maia, Rita CC, Rolim, Hercília ML, Galba, MC (2013). Cadmium tolerance and removal from Cunninghamella elegans related to the polyphosphate metabolism. Int J Mol Sci 14(4):7180–7192. doi:https://doi.org/10.3390/ijms14047180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Do Carmo JR, Pimenta CJ, da Silva JF, de Souza SMC (2013) Recovery of copper (II) absorbed in biomass of Cladosporium cladosporioides. SciAgric 70:3. org:10.1590/S0103-90162013000300002

    Google Scholar 

  • Dursun AY (2008) A comparative study on determination of the equilibrium, kinetic and thermodynamic parameters of biosorption of copper (II) and lead (II) ions onto pretreated Aspergillus niger. Biochem. Eng J 28:187–195. doi:org/10.1016/j.bej.2005.11.003

    Google Scholar 

  • Elanvogvan R, Philip L, Chandraraj K (2010) Hexavalent chromium reduction by free and immobilized cell-free extract of Arthrobacter rhombi-RE. Appl Biochem Biotechnol 160(1):81–97. doi:org/10.1007/s12010-008-8515-6

    Article  Google Scholar 

  • El-Morsy EM (2004) Cunninghamella echinulata a new biosorbent of metal ions from polluted water in Egypt. Mycologia 96:1183–1189

    Article  CAS  Google Scholar 

  • Elsilk SE, Abd El-Raheem R, El-Shanshoury APS (2014) Accumulation of some heavy metal resistant avirulent Bacillus anthracis PS2010 isolated from Egypt. Afr J Micro Res 8(12):1266–1276. doi:10.5897/AJMR2013.6551

    Article  CAS  Google Scholar 

  • Essam F, Jumaily BH, Saleh BH, Shalal M, Hussain SM (2013) Determination of lethal dose (LD50)of exotoxin a from Pseudomonasaeruginosa26A in mice histopathology. IOSR J Pharm Biol Sci 7(6):49–54

    Google Scholar 

  • Ezzourhi L, Castro E, Moya M (2009) Heavy metal tolerance of filamentous fungi isolated from polluted sites in tangier, Morocco. Afr J Microbiol Res 3:35–48. doi.org/10.7745/KJSSF.2012.45.4.565

    Google Scholar 

  • Freitas AC, Ferreira F, Costa AM, Pereira R, Antunes SC, Gonçalves F, Rocha-Santos TAP, Diniz MS, Castro L, Peres I, Duarte AC (2009) Biological treatment of the effluent from a bleached kraft pulp mill using basidiomycete and zygomycete fungi. Sci Total Environ 407:3282–3289. doi:org/10.1016/j.scitotenv.2009.01.054

    Article  CAS  Google Scholar 

  • Gao Y, Miao C, Xia J, Mao L, Wang Y, Zhou P (2012) Plant diversity reduces the effect of multiple heavy metal pollution on soil enzyme activities and microbial community structure. Front Environ Sci En 6(2):213–223. doi:10.1007/s11783-011-0345-z

    Article  CAS  Google Scholar 

  • Gao S, Zhang WB, Sheng XF, He LY, Huang Z (2015) Chitinophaga longshanensis sp. nov., a mineral-weathering bacterium isolated from weathered rock. Int J Syst Evol Microbiol 65:418–423. doi:10.1099/ijs.0.067249-0

    Article  CAS  PubMed  Google Scholar 

  • Ghorbani Y, Oliazadeh M, Shahvedi A (2007) Use of some isolated fungi in biological leaching of aluminum from low grade bauxite. Afr J Biotech 11:1284–1288. doi:10.5897/AJB2007.000-2178

    Article  Google Scholar 

  • Gilman JC (1957) A manual of soil fungi. Iowa State Univ Press, Ames, p 450

    Google Scholar 

  • Grison CM, Jackson S, Merlot S, Dobson A, Grison C (2015) Rhizobium metallidurans sp. nov., a symbiotic heavy metal resistant bacterium isolated from the Anthyllis vulneraria Zn-hyperaccumulator. Int J Syst Evol Microbiol 65:1525–1530. doi:10.1099/ijs.0.000130

    Article  CAS  PubMed  Google Scholar 

  • Gupta K, Chatterjee C, Gupta B (2012) Isolation and characterization of heavy metal tolerant Gram-positive bacteria with bioremedial properties from municipal waste rich soil of Kestopur canal (Kolkata)est Bengal, India. Biologia 67(5):827–836. doi:10.2478/s11756-012-0099-5

    Article  CAS  Google Scholar 

  • Gupta R, Kumar T, Mittal A (2016) Isolation, identification and characterization of heavy metal resistant bacteria from soil of an iron industry, Haryana (India). IJPSR 7(3):1308–1313. doi:10.13040/IJPSR.0975-8232.7(3).1308-13

    Article  CAS  Google Scholar 

  • Hao X, Taghavi S, Xie P, Orbach J, Alwathnani HA, Rensing C, Wei G (2014) Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. Int J Phytoremed 16(2):179–202. https://doi.org/10.1080/15226514.2013.773273

    Article  Google Scholar 

  • Harriso JJ, Ceri H, Raymond JT (2007) Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5:928–938. doi:10.1038/nrmicro1774

    Article  CAS  Google Scholar 

  • Hayat S, Ahmed I, Ahmed A, Samiullah IA (2002) Effect of long-term application of oil refinery wastewater on soil health with special reference to microbiological characteristics. Bioresour Technol 84:159–163. doi:10.1016/S0960-8524(02)00027-5

    Article  CAS  PubMed  Google Scholar 

  • Hemida M, Morsy FM, El-Enany AE, Ohyama T (2012) Isolation and characterization of a heavy-metal-resistant isolate of Rhizobium leguminosarum viciae potentially applicable for biosorption of Cd2+ and Co2+. IntBiodeterBiodegr 67:48–55. doi:10.1016/j.ibiod.2011.10.008

    Article  CAS  Google Scholar 

  • Hijri M, Bell TH, Hassan S, Lauron-Moreau A, Al-Otaibi F (2014) Linkage between bacterial and fungal rhizosphere communities in hydrocarbon-contaminated soils is related to plant phylogeny. ISME J 8:331–334. doi:10.1038/ismej.2013.149

    Article  CAS  PubMed  Google Scholar 

  • Hirak RD, Das S (2014). Bioremediation potential of mercury by Bacillus species isolated from marine environment and wastes of steel industry. Biorem J.18(3):204–212. doi.org/10.1080/10889868.2014.899555

    Google Scholar 

  • Inga Z (2013) Study of the interaction of metals (Hg, Cr, Zn, Ag, Au) with Arthrobacter genera and Spirulina platensis. PhD thesis

    Google Scholar 

  • Iram S, Parveen K, Usman J, Nasir K, Akhtar N, Arouj S, Ahmed I (2012) Heavy metal tolerance of filamentous fungal strains isolated from soil irrigated with industrial wastewater. Biologija 58(3):107–116. doi:org/10.6001/biologija.v58i3.2527

    Article  CAS  Google Scholar 

  • Issazadeh K, Jahanpour N, Pourghorbanali F, Raeisi G, Faekhondeh J (2013) Heavy metals resistance by bacterial strains. Ann Biol Res 4(2):60–63

    Google Scholar 

  • Jaeckel P, Krauss GJ, Krauss G (2005) Cadmium and zinc response of the fungi Heliscus lugdunensis and Verticillium cf. alboatrum isolated from highly polluted water. Sci. Total Environ 346:274–279. doi:10.1016/j.scitotenv.2004.12.082

    Article  CAS  Google Scholar 

  • Juliana RDC, Pimenta CJ, Silva JF, Souza SMC (2013) Recovery of copper (II) absorbed in biomass of Cladosporium cladosporioides. Sci Agric 70(3):147–151. doi:org/10.1590/S0103-90162013000300002

    Article  Google Scholar 

  • Kanmami P, Aravind J, Preston D (2012) Remediation of chromium contaminants using bacteria. Int J Environ Sci Technol 9(1):183–193. doi:10.1007/s13762-011-0013-7

    Article  CAS  Google Scholar 

  • Karelová E, Harichová J, Stojnev T, Pangallo D, Ferianc P (2011) The isolation of heavy-metal resistant culturable bacteria and resistance determinants from a heavy-metal contaminated site. Biologia 66:18–26. doi:10.2478/s11756-010-0145-0

    Article  CAS  Google Scholar 

  • Karn SK, Reddy S (2012) Degradation of 2, 4,6-trichlorophenol by bacteria isolated from secondary sludge of a pulp and paper mill. J Gen Appl Microbiol 58:413–420. doi:org/10.2323/jgam.58.413

    Article  CAS  Google Scholar 

  • Khan AG (2000) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. JTraceElemMedBiol 18:355–364. doi:10.1007/s11356-015-4471-1

    Article  CAS  Google Scholar 

  • Kumar R, Singh P, Dhir B, Sharma AK, Mehta D (2014) Potential of some fungal and bacterial species in bioremediation of heavy metals. Journal of Nuclear Physics, Material Sciences, Radiation and Application 1(2):212–223

    Google Scholar 

  • Kuykendall LD, Young J, Martinez-Romero E, Kerr A, Sawada H (2005) Genus I. Rhizobium. In: Garrity GM, Brenner DJ, Krieg NR, Staley J (eds) Bergey’s manual of systematic bacteriology, vol 2. Springer: Verlag, New York, pp 325–340

    Chapter  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics (modern microbiological methods). Wiley, New York, pp 115–175

    Google Scholar 

  • Lee DW, Lee JE, Lee SD (2009) Chitinophaga rupis sp. nov., isolated from soil. Int J Syst Evol Microbiol 59:2830–2833. doi:10.1099/ijs.0.011163-0

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Cho K, Lim J, Kim W, Hwang S (2011a) Acclimation and activity of ammonia-oxidizing bacteria with respect to variations in zinc concentration, temperature, and microbial population. Bioresour Technol 102:4196–4203. doi:10.1016/j.biortech.2010.12.035

    Article  CAS  PubMed  Google Scholar 

  • Lee M, Ten LN, Woo SG, Park J (2011b) Agromyces soli sp. nov., isolated from farm soil. Int. J Syst Evol Microbiol 61:1286–1292. doi:10.1155/2013/831308

    Article  CAS  Google Scholar 

  • Long F, Su CC, Lei HT, Bolla JR, Do SV, Yu EW (2012) Structure and mechanism of the tripartite CusCBA heavy-metal efflux complex. Philos Trans R Soc Lond Ser B Biol Sci 367:1047–1058. doi:10.1098/rstb.2011.0203

    Article  CAS  Google Scholar 

  • Ma Y, Oliveira RS, Freitas H, Zhang C (2016) Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. FrontPlant Sci 7:918. doi:org/10.3389/fpls.2016.00918

    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  PubMed  Google Scholar 

  • Malgorzata JK, Rosikon K., Fijalkowski K, Grobelak A (2014).The effect of Trichoderma on heavy metal mobilityand uptake by Miscanthus giganteus, Salix sp., Phalaris arundinaceaand Panicumvirgatum.Appl Environ Soil Sci.1–10. doi.org/10.1155/2014/506142

    Google Scholar 

  • Malik A (2004) Metal bioremediation through growing cells. Environ Int 30:261–278. doi:10.1016/j.envint.2003.08.001

    Article  CAS  PubMed  Google Scholar 

  • Mandal SM, Bhattacharyya R (2012) Rhizobium-legume Symbiosis: a model system for the recovery of metal-contaminated agricultural land. In: Zaidi A, Wani PA, Khan MS (eds) Toxicity of heavy metals to legumes and bioremediationol.12.Springer, New York, pp 115–127

    Chapter  Google Scholar 

  • Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin P, Taghavi S, Dunn J, van der Lelie D, Wattiez R (2003) Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol 9:1181–1191. doi:10.1016/S0168-6445(03)00045-7

    Article  CAS  Google Scholar 

  • Mindlin S, Petrenko A, Kurakov A, Beletsky A, Mardanov A, Petrova M (2016) Resistance of permafrost and modern Acinetobacter lwoffii strains to heavy metals and arsenic revealed by genome analysis. Biomed Res Int. doi:org/10.1155/2016/3970831

    Article  Google Scholar 

  • Mohamed HA, Morsy FM, Enamy AWE, Ohyama (2012) Isolation and characterization of a heavy-metal-resistant isolate of Rhizobium leguminosarum bv. viciae potentially applicable for biosorption of Cd2+ and Co2+. Int Biodeter Biodegr 67:48–55. doi:10.1016/j.ibiod.2011.10.008

    Article  CAS  Google Scholar 

  • Mondani L, Piette L, Christen R, Bachar D, Berthomieu C, Chapon V (2012) Microbacterium lemovicicum sp. nov., a bacterium isolated from a natural uranium-rich soil. IntJSystEvolMicrobiol 63:2600–2606. doi:10.1007/s00203-015-1183-3

    Article  CAS  Google Scholar 

  • Nies DH (1995) The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J Bacteriol 177:2707–2712

    Article  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy metal resistance. ApplMicrobial Biotechnol 51:730–750. doi:10.1007/s002530051457

    Article  CAS  Google Scholar 

  • Olukoya DK, Smith SI, Hori MO (1997) Isolation and characterization of heavy metal resistant bacteria from Lagos lagoon folia. Microbiol 42(5):441–444. doi:10.1007/BF02826550

    Article  CAS  Google Scholar 

  • Osborn AM, Bruce KD, Strike P, Ritchie DA (1997) Distribution, diversity and evolution of the bacterial mercury resistance (mer) operon. FEMS Microbiol Rev 19:239–262. doi:http://dx.doi.org/10.1111/j.1574-6976

  • Pal A, Choudhuri P, Dutta S, Mukherjee PK, Paul AK (2004) Isolation and characterization of nickel-resistant microflora from serpentine soils of Andaman. World J Microbiol Biotech 20:881–886. doi:10.1007/s11274-004-2776-1

    Article  CAS  Google Scholar 

  • Palanivel VP, Shim J, You Y, Choi S, Seralathan KK, Lee KJ, Kim HJ, Oh BT(2010). Removal of zinc by live, dead, and dried biomass of Fusarium spp. isolated from the abandoned-metal mine in South Korea and its perspective of producing nanocrystals. J Haz Mat. 182(1–3):317–324.doi:org/10.1016/j.jhazmat.2010.06.032

    Article  CAS  PubMed  Google Scholar 

  • Paris D, Blondeau R (1999) Isolation and characterization of Arthrobacter sp. from activated sludge of a pulp and paper mill. Water Res 33(4):947–950. doi:org/10.1016/S0043-1354(98)00298-X

    Article  CAS  Google Scholar 

  • Park SK, Kim MS, Jung MJ, Nam YD, Park EJ, Roh SW, Bae JW (2011) Brachybacterium squillarum sp. nov., isolated from salt-fermented seafood. Int J Syst Evol Microbiol 61:1118–1122. https://doi.org/10.1099/ijs.0.022517-0

    Article  Google Scholar 

  • Pattus F, Abdallah M (2000) Siderophores and iron-transport in microorganisms: review. J Chin Chem Soc 47:1–20. doi:10.1002/jccs.200000001

    Article  CAS  Google Scholar 

  • Petrovic JJ, Danilovic G, Curcic N, Milinkovic M, Stosic N, Pankovic D, Raicevic V (2014) Coppertolerance of Trichoderma species. Arch Biol Sci Belgrade 66(1):137–142. https://doi.org/10.2298/ABS1401137J

    Article  Google Scholar 

  • Piccirillo C, Pereira SIA, Marques APGC, Pullar RC, Tobaldi DM, Pintado ME, Castro PML (2013) Bacteria immobilization on hydroxyapatite surface for heavy metals removal. J Environ Manag 121:87–95. doi:org/10.1016/j.jenvman.2013.02.036

    Article  CAS  PubMed  Google Scholar 

  • Piotrowska-Seget Z, Cycon, M, Kozdroj J (2005) Metal tolerant bacteria occurring in heavily polluted soil and mine spoil. Appl Soil Ecol. 28:237–246. doi:org/10.1016/j.apsoil.2004.08.001

    Article  Google Scholar 

  • Rajbanshi A (2008) Study on heavy metal resistant bacteria in Guheswori sewage treatment plant. Our Nature 6:52–57. doi:10.3126/on.v6i1.1655

    Article  Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potentialof siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28:142–149. doi:org/10.1016/j.tibtech.2009.12.002

    Article  CAS  PubMed  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv. 30(6):1562–1574.doi:org/10.1016/j.biotechadv.2012.04.011

    Article  CAS  PubMed  Google Scholar 

  • Rao KR, Rashmi K, Latha JNL (2005) Bioremediation of toxic metal ions using biomass of Aspergillus fumigates from fermentative waste. Indian J Biotechnol 4:139–143. http://hdl.handle.net/123456789/5627

    Google Scholar 

  • Raper KB, Fennell DJ (1965) The genus Aspergillus. Williams and Wilkins, Baltimore, p 686

    Google Scholar 

  • Rathnayake VN, Megharaj M, Bolan N, Naidu R (2009) Tolerance of heavy metals by gram positive soil bacteria. WASET 53:1185–1189

    Google Scholar 

  • Reeve WG, Tiwari RP, Kale NB, Dilworth MJ, Glenn AR (2002) ActP controls copper homeostasis in Rhizobium leguminosarum bv. viciae and Sinorhizobium meliloti preventing low pH-induced copper toxicity. Mol Biol 43(4):981–991. doi:10.1046/j.1365-2958.2002.02791.x

    Article  CAS  Google Scholar 

  • Rhodes CJ (2013) Applications of bioremediation and phytoremediation. Sci Prog. 96(4): 417–427.doi:org/10.3184/003685013X13818570960538

    Article  CAS  PubMed  Google Scholar 

  • Rosales E, Pazos M, Sanroman MA, Tavares T (2012) Application of zeolite-Arthrobacter viscosus system for the removal of heavy metal and dye: chromium and azure B. Desalination. 284:150–156. doi:org/10.1016/j.desal.2011.08.049

    Article  CAS  Google Scholar 

  • Rouhollahi F, Zamani A, Karimi K, Etesami N (2014) Enhancement of nickel biosorption on fungal biomass by enzymatic and alkali pretreatments. Int J Environ Sci Technol. doi:10.1007/s13762-014-0624-x

    Article  CAS  Google Scholar 

  • Sahoo KN, Pakshirajan K, Ghosh PK (2014) Evaluation of 4-bromophenol biodegradation in mixed pollutants system by Arthrobacter chlorophenolicus A6 in an upflow packed bed reactor. Biodegradation 25(5):705–718. doi:10.1007/s10532-014-9693-2

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstruction phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Santa CL, Gonzalez-Lopez J, Manzanera M (2013) Arthrobacter siccitolerans sp. nov., a highly desiccation-tolerant, xeroprotectant-producing strain isolated from dry soil. Int J Syst Evol Microbiol 63:4174–4180. doi:10.1099/ijs.0.052902-0

    Article  CAS  Google Scholar 

  • Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854. doi:10.1111/j.1462-2920.2011.02556.x

    Article  CAS  PubMed  Google Scholar 

  • Sen M (2011) Biosorption of Cr (VI) by resting cells of Fusarium solani Iran. J Environ Health SciEng 8(2):117–120. doi:10.4236/ojapps.2012.23021

    Article  CAS  Google Scholar 

  • Shivkumar CK, Thippeswamy B, Krishnappa M, Ananthamurthy KS (2011) Bioaccumulation potency of ecotoxic heavy metals by indigenous Rhizopus and Penicillium sp: a comparative study. J Pure. Appl Microbiol 6(1):231–239

    Google Scholar 

  • Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60(100):182–194. doi:10.3389/fpls.2016.00918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith KS, Balistrieri LS, Todd AS (2015) Using biotic ligand models to predict metal toxicity in mineralized systems. Appl Geochem 57:55–72. doi:10/1016/j.apgeochem.2014.07.005

    Article  CAS  Google Scholar 

  • Song N, Ma Y, Zhao Y, Tang S (2015) Elevated ambient carbon dioxide and Trichoderma inoculum could enhance cadmium uptake of Lolium perenne explained by changes of soil pH, cadmium availability and microbial biomass. Appl Soil Ecol 85:56–64. doi:10.1016/j.apsoil.2014.09.007

    Article  Google Scholar 

  • Stan V, Gament E, Cornea CP, Voaideş C, Duşa M, Plopeanu G (2011) Effects of heavy metal from polluted soils on the Rhizobium diversity. Not Bot Hort Agrobot Cluj 39(1):88–95. doi:http://dx.doi.org/10.15835/nbha3916081

    Article  CAS  Google Scholar 

  • Stefanowicz AM, Niklińska M, Kapusta P, SzarekŁukaszewska G, Grodzińska K (2010).Metal pollution, soil properties and plant diversity as determinants of bacterial and fungal performance in soils. In: 15th ICHMET, pp 708–712

    Google Scholar 

  • Sun F, Shao Z (2007) Biosorption and bioaccumulation of lead by Penicillium sp. Psf-2 isolated from the deep sea sediment of the Pacific Ocean. Extremophiles 11:853–858. doi:10.1007/s00792-007-0097-7

    Article  PubMed  Google Scholar 

  • Swer PB, Joshi SR, Acharya C (2016) Cesium and strontium tolerant Arthrobacter sp. strain KMSZP6 isolated from a pristine uranium ore deposit. AMB Expr 6:69. doi:10.1186/s13568-016-0247-3

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121.pmid: 21546353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tappe W, Herbst M, Hofmann D, Koeppchen S, Kummer S, Thiele B (2013) Degradation of sulfadiazine by Microbacterium lacus strain SDZm4, isolated from lysimeters previously manured with slurry from sulfadiazine-medicated pigs. Appl Environ Microb 79(8):2572–2577. doi:10.1128/AEM.03636-12 pmid:23396336

    Article  CAS  Google Scholar 

  • Teng Y, Luo Y, Ma W, Zhu L, Ren W, Luo Y. Li, Z (2015). Trichoderma reesei FS10-C enhances phytoremediation of cd-contaminated soil by Sedum plumbizincicola and associated soil microbial activities. Front Plant Sci. 9: 220. doi.org/10.3389/fpls.2015.00438

    Google Scholar 

  • Thakre NA, Shanware AS (2015) Promising biological indicator of heavy metal pollution: bioluminescent bacterial strains isolated and characterized from marine niches of Goa, India. Indian J Microbiol 55(3):327–332. doi:10.1007/s12088-015-0531-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thawai C, Tanasupawat S, Suwanborirux K, Kudo T (2011) Agromyces tropicus sp. nov., isolated from soil. Int J Syst Evol Microbiol 61:605–609. doi:10.1099/ijs.0.021774-0

    Article  CAS  PubMed  Google Scholar 

  • Thippeswamy B, Shivakumar CK, Krishnappa M (2012) Accumulation potency of heavy metals by Saccharomyces sp. indigenous to paper mill effluent. J Env Res Develop 6(3):439–445

    CAS  Google Scholar 

  • Thippeswamy B, Shivakumar CK, Krishnappa M (2014) Optimization of heavy metals bioaccumulation in Aspergillus niger and Aspergillus flavus. Int J Environ Biol 4(2):188–195

    Google Scholar 

  • Tripathi AK, Harsh NSK, Gupta N (2007) Fungal treatment of industrial effluents: a mini-review. Life Science Journal 4(2):78–81

    CAS  Google Scholar 

  • Tunali S, Cabuk A, Akar T (2006) Removal of lead and copper ions from aqueous solutions by bacterial strain isolated from soil. ChemEngJ 115(3):203–211. doi:10.1016/j.cej.2005.09.023

    Article  CAS  Google Scholar 

  • Turner S, Pryer KM, Miao VPW (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338. doi:10.1111/j.1550-7408.1999.tb04612.x

    Article  CAS  PubMed  Google Scholar 

  • Ullah A, Heng S, Munis MFH, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40. doi:10.1016/j.envexpbot.2015.05.001

    Article  CAS  Google Scholar 

  • Valix M, Tang JY, Malik R (2001) Heavy metal tolerance of fungi. Miner Eng 14:499–505. doi:10.1016/S0892-6875(01)00037-1

    Article  CAS  Google Scholar 

  • Van DB, Christov L (2002) Adsorption of colour from bleach plant effluent using biomass and cell wall fractions from Rhizomucor pusillus. J Chem Technol Biotechnol 77:155–158. doi:10.1002/jctb.535

    Article  CAS  Google Scholar 

  • Verma P, Singh S, Verma RK (2016) Heavy metal biosorption by Fusarium strains isolated from iron ore mines overburden soil. IntJEnvironSci Toxicol Res 4(4):61–69

    Google Scholar 

  • Volesky B, Holan ZR (1995) Biosorption of heavy metals. Biotechnol Prog 11:235–250. doi:10.1021/bp00033a001

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Shao Z, Liu Y, Wang G (2009) Removal of multi-heavy metals using biogenic manganese oxides generated by a deep-sea sedimentary bacterium - Brachybacterium sp. strain Mn32. Microbiology 155:1989–1996. doi:10.1099/mic.0.024141-0

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Cheng C, He LY, Huang Z (2014) Chitinophaga jiangningensis sp. nov., a mineral-weathering bacterium. Int J Syst Evol Microbiol 64:260–265. doi:10.1099/ijs.0.067249-0

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, LeeS TJ (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for Phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Willie JG, Peijnenburg M, Zablotskaja M, Martina GV (2007) Monitoring metals in terrestrial environments within a bioavailability framework and a focus on soil extraction. Ecotox Environmen Safe 67(2):163–179. doi:10.1016/j.ecoenv.2007.02.008

    Article  CAS  Google Scholar 

  • Wu SC, Cheung KC, Luo YM, Wong MH (2006) Effects of inoculation of plant growth-promoting rhizobacteria on metal uptake by Brassica juncea. Environ Pollut 140:124–135. doi:10.1016/j.envpol.2005.06.023

    Article  CAS  PubMed  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecology. doi: org/10.5402/2011/402647

    Article  Google Scholar 

  • Yang HB, Tan N, Wu FJ, Liu HJ, Sun M, She ZG, Lin YC (2012) Biosorption of uranium (VI) by mangrove endophytic fungus Fusarium sp. ZZF51 from the South China Sea. J Radioanal Nucl Chem 292(3):1011–1016. doi:10.1007/s10967-011-1552-6

    Article  CAS  PubMed  Google Scholar 

  • Yasir M, Chung EJ, Song GC, Bibi F, Jeon CK, Chung YR (2011) Chitinophaga eiseniae sp. nov., isolated from vermicompost. Int J Syst Evol Microbiol 61:2373–2378. doi:10.1099/ijs.0.040014-0

    Article  CAS  PubMed  Google Scholar 

  • Yazdani MF, Abdullah CKY, Tan SG (2009) Trichoderma atroviride as a bioremediatorof cu pollution: an in vitro study. Toxicol Environ Chem 91(7):1305–1314. doi:10.1080/02772240802616510

    Article  CAS  Google Scholar 

  • Yu X, Li Y, Zhang C, Liu H, Liu J, Zheng W, Kang X, Qiang C (2014) Culturable heavy metal-resistant and plant growth promoting bacteria in V-Ti magnetite mine tailing soil from Panzhihua, China. PLoS One 9(9):e106618. doi:10.1371/journal.pone.0106618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zafar S, Aqil F, Ahmad I (2007) Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agriculture soil. Bioresour Technol 98:2557–2561. doi:10.1016/j.biortech.2006.09.051

    Article  CAS  PubMed  Google Scholar 

  • Zhang YF, He LY, Chen ZJ, Zhang WH, Wang QY, Qian M (2011) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:720–725. doi:10.1016/j.jhazmat.2010.12.069

    Article  CAS  Google Scholar 

  • Zhang X, Lin L, Chen M, Zhu Z, Yang W, Chen B, Yang X, An Q (2012) A nonpathogenic Fusarium oxysporum strain enhances phytoextraction of heavy metals by the hyperaccumulator sedum alfredii Hance. J Hazard Mater 229-230:361–370. doi:10.1016/j.jhazmat.2012.06.013

    Article  CAS  PubMed  Google Scholar 

  • Zhou Q, Chen Y, Yang M, Li W, Deng L (2013) Enhanced bioremediation of heavy metal from effluent by sulfate-reducing bacteria with copper-iron bimetallic particles support. Bioresour Technol 136:413–417. doi:10.1016/j.biortech.2013.03.047

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Commonwealth Scholarship grant, Canada, for carrying out the present work in the Department of Biological Science, University De Montreal, Montreal, and Genome Quebec Innovation Centre, Canada, for getting the accession numbers of all isolated trace metal-tolerant microbial strains.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dhritiman Chanda .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Chanda, D., Sharma, G.D., Jha, D.K., Hijri, M. (2017). Tolerance of Microorganisms in Soil Contaminated with Trace Metals: An Overview. In: Shukla, P. (eds) Recent advances in Applied Microbiology . Springer, Singapore. https://doi.org/10.1007/978-981-10-5275-0_8

Download citation

Publish with us

Policies and ethics