Skip to main content
Log in

Enhanced bioremediation of lead-contaminated soil by Solanum nigrum L. with Mucor circinelloides

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Strain selected from mine tailings in Anshan for Pb bioremediation was characterized at the genetic level by internal transcribed spacer (ITS) sequencing. Results revealed that the strain belongs to Mucor circinelloides. Bioremediation of lead-contaminated soil was conducted using Solanum nigrum L. combined with M. circinelloides. The removal efficacy was in the order microbial/phytoremediation > phytoremediation > microbial remediation > control. The bioremediation rates were 58.6, 47.2, and 40.2% in microbial/phytoremediation, microbial remediation, and phytoremediation groups, respectively. Inoculating soil with M. circinelloides enhanced Pb removal and S. nigrum L. growth. The bioaccumulation factor (BF, 1.43), enrichment factor (EF, 1.56), and translocation factor (TF, 1.35) were higher than unit, suggesting an efficient ability of S. nigrum L. in Pb bioremediation. Soil fertility was increased after bioremediation according to change in enzyme activities. The results indicated that inoculating S. nigrum L. with M. circinelloides enhanced its efficiency for phytoremediation of soil contaminated with Pb.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adhikari T, Kumar A, Singh MV, Rao AS (2010) Phytoaccumulation of lead by selected wetland plant species. Commun Soil Sci Plant Anal 41:2623–2632

    Article  CAS  Google Scholar 

  • Ahsan N, Renaut J, Komatsu S (2009) Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics 9:2602–2621

    Article  CAS  Google Scholar 

  • Albarracín VH, Amoroso MJ, Abate CM (2010) Bioaugmentation of copper polluted soil microcosms with Amycolatopsis tucumanensis to diminish phytoavailable copper for Zea mays plants. Chemosphere 79:131–137. doi:10.1016/j.chemosphere.2010.01.038

    Article  Google Scholar 

  • Alkorta I, Garbisu C (2001) Phytoremediation of organic contaminants in soils. Bioresour Technol 79:273–276

    Article  CAS  Google Scholar 

  • Babu AG, Kim JD, Oh BT (2013) Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. J Hazard Mater 250–251:477–483

    Article  Google Scholar 

  • Bahadir T, Bakan G, Altas L, Buyukgungor H (2007) The investigation of lead removal by biosorption: an application at storage battery industry wastewaters. Enzyme Microb Technol 41:98–102

    Article  CAS  Google Scholar 

  • Bai H-J, Zhang Z-M, Yang G-E, Li B-Z (2008) Bioremediation of cadmium by growing Rhodobacter sphaeroides: kinetic characteristic and mechanism studies. Bioresour Technol 99:7716–7722. doi:10.1016/j.biortech.2008.01.071

    Article  CAS  Google Scholar 

  • Banerjee R, Goswami P, Pathak K, Mukherjee A (2016) Vetiver grass: an environment clean-up tool for heavy metal contaminated iron ore mine-soil. Ecol Eng 90:25–34. doi:10.1016/j.ecoleng.2016.01.027

    Article  Google Scholar 

  • Bang J et al (2015) Phytoremediation of heavy metals in contaminated water and soil using sp. Goedae-Uksae 1

    Google Scholar 

  • Barea JM, Azcon-Aguilar C, Azcon R (1997) Interactions between mycorrhizal fungi and rhizosphere microorganisms within the context of sustainable soil-plant systems

    Google Scholar 

  • Baycu G, Tolunay D, Özden H, Günebakan S (2006) Ecophysiological and seasonal variations in Cd, Pb, Zn, and Ni concentrations in the leaves of urban deciduous trees in Istanbul. Environ Pollut 143:545–554

    Article  CAS  Google Scholar 

  • Borowik A, Wyszkowska J, Kucharski M, Kucharski J (2014) Resistance of dehydrogenases, catalase, urease and plants to soil contamination with zinc. J Elementology 19:4

    Google Scholar 

  • Boureux A, Vignal E, Faure S, Fort P (2007) Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol Biol Evol 24:203–216

    Article  CAS  Google Scholar 

  • Branquinho C, Serrano HC, Pinto MJ, Martinsloução MA (2007) Revisiting the plant hyperaccumulation criteria to rare plants and earth abundant elements. Environ Pollut 146:437–443

    Article  CAS  Google Scholar 

  • Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286

    Article  Google Scholar 

  • Cederkvist K, Ingvertsen ST, Jensen MB, Holm PE (2013) Behaviour of chromium(VI) in stormwater soil infiltration systems. Appl Geochem 35:44–50. doi:10.1016/j.apgeochem.2013.05.011

    Article  CAS  Google Scholar 

  • Chang Y-S, Huang H-D, Yeh K-T, Chang J-G (2016) Genetic alterations in endometrial cancer by targeted next-generation sequencing. Exp Mol Pathol 100:8–12. doi:10.1016/j.yexmp.2015.11.026

    Article  CAS  Google Scholar 

  • Chaudhry Q, Blom-Zandstra M, Gupta SK, Joner E (2005) Utilising the synergy between plants and rhizosphere microorganisms to enhance breakdown of organic pollutants in the environment (15 pp). Environ Sci Pollut Res 12:34–48. doi:10.1065/espr2004.08.213

    Article  CAS  Google Scholar 

  • Cheah YK (2001) Isolation, screening for bioactivities and identification of selected endophyte fungi by sequencing of 18S rRNA/ITS genes

    Google Scholar 

  • Cherkasov AS, Taylor C, Sokolova IM (2010) Seasonal variation in mitochondrial responses to cadmium and temperature in eastern oysters Crassostrea virginica (Gmelin) from different latitudes. Aquat Toxicol 97:68–78. doi:10.1016/j.aquatox.2009.12.004

    Article  CAS  Google Scholar 

  • Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokaikun JF, Mond JJ, Foster SJ (2007) Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189:1025–1035

    Article  CAS  Google Scholar 

  • Daud MK, Ali S, Variath MT, Zhu SJ (2013) Differential physiological, ultramorphological and metabolic responses of cotton cultivars under cadmium stress. Chemosphere 93:2593–2602. doi:10.1016/j.chemosphere.2013.09.082

    Article  CAS  Google Scholar 

  • Dick RP (1997) Soil enzyme activities as integrative indicators of soil health

    Google Scholar 

  • Dimkpa CO, Svatoš A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19–25. doi:10.1016/j.chemosphere.2008.09.079

    Article  CAS  Google Scholar 

  • Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil–rhizosphere–plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99:259–278

    Article  CAS  Google Scholar 

  • Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279

    Article  CAS  Google Scholar 

  • Galal TM, Shehata HS (2015) Bioaccumulation and translocation of heavy metals by Plantago major L. grown in contaminated soils under the effect of traffic pollution. Ecol Indic 48:244–251. doi:10.1016/j.ecolind.2014.08.013

    Article  CAS  Google Scholar 

  • Ghavri SV, Bauddh K, Kumar S, Singh RP (2013) Bioaccumulation and translocation potential of Na + and K+ in native weeds grown on industrially contaminated soil. Int J Chem Res 5:1869–1875

    CAS  Google Scholar 

  • Ghosh M, Singh SP (2005) A comparative study of cadmium phytoextraction by accumulator and weed species. Environ Pollut 133:365–371

    Article  CAS  Google Scholar 

  • Gülser F, Erdoğan E (2008) The effects of heavy metal pollution on enzyme activities and basal soil respiration of roadside soils. Environ Monit Assess 145:127–133

    Article  Google Scholar 

  • Guo H et al (2010) Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. Bioresour Technol 101:8599–8605. doi:10.1016/j.biortech.2010.06.085

    Article  CAS  Google Scholar 

  • Gupta S, Nayek S, Saha RN, Satpati S (2008) Assessment of heavy metal accumulation in macrophyte, agricultural soil, and crop plants adjacent to discharge zone of sponge iron factory. Environ Geol 55:731–739

    Article  CAS  Google Scholar 

  • Gupta DK, Huang HG, Corpas FJ (2013) Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res 20:78–85

    Google Scholar 

  • Hao X, Xie P, Johnstone L, Miller SJ, Rensing C, Wei G (2012) Genome sequence and mutational analysis of plant-growth-promoting bacterium Agrobacterium tumefaciens CCNWGS0286 isolated from a zinc-lead mine tailing. Appl Environ Microbiol 78:5384–5394

    Article  CAS  Google Scholar 

  • Jiang W, Fan W (2008) Bioremediation of heavy metal-contaminated soils by sulfate-reducing bacteria. Ann N Y Acad Sci 1140:446–454

    Article  CAS  Google Scholar 

  • Kamran MA et al (2014) The potential of the flora from different regions of Pakistan in phytoremediation: a review. Environ Sci Pollut Res Int 21:150–152

    Article  Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72

    Article  CAS  Google Scholar 

  • Kang C-H, Oh SJ, Shin Y, Han S-H, Nam I-H, So J-S (2015) Bioremediation of lead by ureolytic bacteria isolated from soil at abandoned metal mines in South Korea. Ecol Eng 74:402–407. doi:10.1016/j.ecoleng.2014.10.009

    Article  Google Scholar 

  • Karaca A, Naseby DC, Lynch JM (2002) Effect of cadmium contamination with sewage sludge and phosphate fertiliser amendments on soil enzyme activities, microbial structure and available cadmium. Biol Fertil Soils 35:428–434

    Article  CAS  Google Scholar 

  • Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364

    Article  CAS  Google Scholar 

  • Kızılkaya RI, Dengi̇z O (2010) Variation of land use and land cover effects on some soil physico-chemical characteristics and soil enzyme activity. Zemdirbyste-Agriculture 97:15–24

    Google Scholar 

  • Kotaś J, Stasicka Z (2000) Chromium occurrence in the environment and methods of its speciation. Environ Pollut 107:263–283. doi:10.1016/S0269-7491(99)00168-2

    Article  Google Scholar 

  • Lam TV, Agovino P, Niu X, Roché L (2007) Linkage study of cancer risk among lead-exposed workers in New Jersey. Sci Total Environ 372:455–462. doi:10.1016/j.scitotenv.2006.10.018

    Article  CAS  Google Scholar 

  • Lannig G, Cherkasov AS, Sokolova IM (2006) Temperature-dependent effects of cadmium on mitochondrial and whole-organism bioenergetics of oysters (Crassostrea virginica). Mar Environ Res 62(Supplement 1):S79–S82. doi:10.1016/j.marenvres.2006.04.010

    Article  CAS  Google Scholar 

  • Li X, Peng W, Jia Y, Lu L, Fan W (2016) Bioremediation of lead contaminated soil with Rhodobacter sphaeroides. Chemosphere 156:228–235

    Article  CAS  Google Scholar 

  • Lipińska A, Wyszkowska J, Kucharski J (2015) Diversity of organotrophic bacteria, activity of dehydrogenases and urease as well as seed germination and root growth Lepidium sativum, Sorghum saccharatum and Sinapis alba under the influence of polycyclic aromatic hydrocarbons. Environ Sci Pollut Res 22:18519–18530. doi:10.1007/s11356-015-5329-2

    Article  Google Scholar 

  • Liu L, Jiang C-Y, Liu X-Y, Wu J-F, Han J-G, Liu S-J (2007) Plant-microbe association for rhizoremediation of chloronitroaromatic pollutants with Comamonas sp. strain CNB-1. Environ Microbiol 9:465–473. doi:10.1111/j.1462-2920.2006.01163.x

    Article  CAS  Google Scholar 

  • Liu H, Guo S, Jiao K, Hou J, Xie H, Xu H (2015) Bioremediation of soils co-contaminated with heavy metals and 2,4,5-trichlorophenol by fruiting body of Clitocybe maxima. J Hazard Mater 294:121–127. doi:10.1016/j.jhazmat.2015.04.004

    Article  CAS  Google Scholar 

  • Luo S et al (2012) Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Appl Microbiol Biotechnol 93:1745–1753

    Article  CAS  Google Scholar 

  • Maier RM, Pepper IL, Gerba CP (2009) Chapter 1–Introduction to Environmental Microbiology. Environ Microbiol 50:3–7

  • Makoi J, Ndakidemi PA (2008) Selected soil enzymes: examples of their potential roles in the ecosystem. Afr J Biotechnol 7:181–191

    CAS  Google Scholar 

  • Marrugo-Negrete J, Durango-Hernández J, Pinedo-Hernández J, Olivero-Verbel J, Díez S (2015) Phytoremediation of mercury-contaminated soils by Jatropha curcas. Chemosphere 127:58–63. doi:10.1016/j.chemosphere.2014.12.073

    Article  CAS  Google Scholar 

  • Mello A, Napoli C, Murat C, Morin E, Marceddu G, Bonfante P (2011) ITS-1 versus ITS-2 pyrosequencing: a comparison of fungal populations in truffle grounds. Mycologia 103:1184–1193

    Article  CAS  Google Scholar 

  • Naik MM, Dubey SK (2013) Lead resistant bacteria: lead resistance mechanisms, their applications in lead bioremediation and biomonitoring. Ecotoxicol Environ Saf 98:1–7. doi:10.1016/j.ecoenv.2013.09.039

    Article  CAS  Google Scholar 

  • Nonnoi F, Chinnaswamy A, Torre VSGDL, Peña TCDL, Lucas MM, Pueyo JJ (2012) Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago spp. and Trifolium spp.) growing in mercury-contaminated soils. Appl Soil Ecol 61:49–59

    Article  Google Scholar 

  • Oleszczuk P, Jośko I, Futa B, Pasieczna-Patkowska S, Pałys E, Kraska P (2014) Effect of pesticides on microorganisms, enzymatic activity and plant in biochar-amended soil. Geoderma 214–215:10–18

    Article  Google Scholar 

  • Openshaw K (2000) A review of Jatropha curcas: an oil plant of unfulfilled promise. Biomass Bioenergy 19:1–15

    Article  Google Scholar 

  • Qian H, Hu B, Wang Z, Xi X, Tao H (2007) Effects of validamycin on some enzymatic activities in soil. Environ Monit Assess 125:1–8

    Article  CAS  Google Scholar 

  • QingRen W, YanShan C, XiuMei L, YiTing D, Peter C (2003) Soil contamination and plant uptake of heavy metals at polluted sites in China. J Environ Sci Health A 38:823

    Article  Google Scholar 

  • Rajkumar M, Freitas H (2008) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71:834–842

    Article  CAS  Google Scholar 

  • Roane TM, Rensing C, Pepper IL, Maier RM (2009) Chapter 21—microorganisms and metal pollutants, Environmental microbiology (Second Edition). Academic, San Diego, pp 421–441. doi:10.1016/B978-0-12-370519-8.00021-3

    Google Scholar 

  • Schoch CL, Consortium FB, Schoch CL et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci U S A 109:6241–6246

    Article  CAS  Google Scholar 

  • Tang YT, Qiu RL, Zeng XW, Ying RR, Yu FM, Zhou XY (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134

    Article  CAS  Google Scholar 

  • Tauqeer HM et al (2015) Phytoremediation of heavy metals by Alternanthera bettzickiana: growth and physiological response. Ecotoxicol Environ Saf 126:138–146

    Article  Google Scholar 

  • Ullah A, Sun H, 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

    Article  CAS  Google Scholar 

  • Wang T et al (2014) The immobilization of heavy metals in soil by bioaugmentation of a UV-mutant Bacillus subtilis 38 assisted by NovoGro biostimulation and changes of soil microbial community. J Hazard Mater 278:483–490. doi:10.1016/j.jhazmat.2014.06.028

    Article  CAS  Google Scholar 

  • Wang Y, Peng B, Yang Z, Chai L, Liao Q, Zhang Z, Li C (2015) Bacterial community dynamics during bioremediation of Cr(VI)-contaminated soil. Appl Soil Ecol 85:50–55. doi:10.1016/j.apsoil.2014.09.002

    Article  Google Scholar 

  • Winquist E et al (2014) Bioremediation of PAH-contaminated soil with fungi – From laboratory to field scale. Int Biodeterior Biodegrad 86, Part C:238–247. doi:10.1016/j.ibiod.2013.09.012

    Article  Google Scholar 

  • Yao Z, Li J, Xie H, Yu C (2012) Review on remediation technologies of soil contaminated by heavy metals. Prog Environ Sci 16:722–729. doi:10.1016/j.proenv.2012.10.099

    Article  CAS  Google Scholar 

  • Zhou W, Leul M (1998) Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regul 26:41–47

    Article  CAS  Google Scholar 

  • Zhou G, Xia X, Wang H, Li L, Wang G, Zheng S, Liao S (2016) Immobilization of lead by Alishewanella sp. WH16-1 in pot experiments of Pb-contaminated paddy soil. Water Air Soil Pollut 227:339

    Article  Google Scholar 

  • Zouboulis AI, Loukidou MX, Matis KA (2004) Biosorption of toxic metals from aqueous solutions by bacteria strains isolated from metal-polluted soils. Process Biochem 39:909–916. doi:10.1016/S0032-9592(03)00200-0

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the financial support received from the Anshan Iron and Steel Technology Project (11161467), the National Natural Science Foundation of P.R. China (20977094), and the Science and Technology Development Plan Projects of Weifang (2014ZJ1055).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhaojie Cui.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, L., Cao, X., Li, M. et al. Enhanced bioremediation of lead-contaminated soil by Solanum nigrum L. with Mucor circinelloides . Environ Sci Pollut Res 24, 9681–9689 (2017). https://doi.org/10.1007/s11356-017-8637-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-8637-x

Keywords

Navigation