Skip to main content
SpringerLink
Log in

Lead accumulation and soil microbial activity in the rhizosphere of the mining and non-mining ecotypes of Athyrium wardii (Hook.) Makino in adaptation to lead-contaminated soils

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

Abstract

Better understanding of microbial activity in the rhizosphere soils associated with lead (Pb) uptake by plants may help with the phytoremediation of Pb-contaminated soils. In this work, the effects of Pb exposure (0, 200, 400, 600, 800 mg kg−1) on Pb accumulation and soil microbial activity in the rhizosphere of the mining ecotype (ME) and corresponding non-mining ecotype (NME) of Athyrium wardii (Hook.) Makino were investigated through a pot experiment. Although the plant growth of the two ecotypes was inhibited under Pb stress, the ME showed a less biomass decrease (12.6–44.0%) for aboveground than the NME, showing a greater tolerance to Pb stress. Pb concentrations as well as Pb accumulation in the two ecotypes showed an increasing trend with increasing soil Pb concentrations. The ME presented greater Pb accumulation ability than the NME, especially in underground parts. Pb availability in the rhizosphere soils of the two ecotypes after harvest decreased compared with those before transplantation. Available Pb in the rhizosphere of the ME was 1.4–4.8 times higher than that of the NME under exposure to 200–800 mg kg−1 Pb. The ME shows a greater ability to mobilize Pb in the rhizosphere soils. Pb exposure resulted in an inhibition of microbial activity in the rhizosphere of the two ecotypes. The ME demonstrated greater soil respiration and microbial biomass carbon (MBC) in the rhizosphere than the NME when treated with 200–800 mg kg−1 Pb. The ME showed a less decrease for MBC and a less increase for metabolic quotient in the rhizosphere soils than the NME when exposed to Pb generally. Microorganisms in the rhizosphere soils of the ME seem to be much more adapted to Pb stress, thus showing a great benefit for Pb accumulation and the phytostabilization of Pb-contaminated soils by the ME.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91(7):869–881

    Article  CAS  Google Scholar 

  • Alvarenga P, Gonçalves AP, Fernandes RM, De Varennes A, Vallini G, Duarte E, Cunha-Queda AC (2009) Organic residues as immobilizing agents in aided phytostabilization:(I) Effects on soil chemical characteristics. Chemosphere 74(10):1292–1300

    Article  CAS  Google Scholar 

  • Andra SS, Datta R, Sarkar D, Makris KC, Mullens CP, Sahi SV, Bach SB (2010) Synthesis of phytochelatins in vetiver grass upon lead exposure in the presence of phosphorus. Plant Soil 326(1–2):171–185

    Article  CAS  Google Scholar 

  • Bolan NS, Park JH, Robinson B, Naidu R, Huh KY (2011) Phytostabilization: a green approach to contaminant containment. In: Advances in agronomy. Academic, Cambridge, pp 145–204

    Google Scholar 

  • Ciarkowska K, Hanus-Fajerska E, Gambuś F, Muszyńska E, Czech T (2017) Phytostabilization of Zn-Pb ore flotation tailings with Dianthus carthusianorum and Biscutella laevigata after amending with mineral fertilizers or sewage sludge. J Environ Manag 189:75–83

    Article  CAS  Google Scholar 

  • Curl EA, Truelove B (1986) The rhizosphere. Springer, Berlin, pp 1–251

    Book  Google Scholar 

  • Dary M, Chamber-Pérez MA, Palomares AJ, Pajuelo E (2010) “In situ” phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177(1–3):323–330

    Article  CAS  Google Scholar 

  • Das S, Chou ML, Jean JS, Yang HJ, Kim PJ (2017) Arsenic-enrichment enhanced root exudates and altered rhizosphere microbial communities and activities in hyperaccumulator Pteris. J Hazard Mater 325:279–287

    Article  CAS  Google Scholar 

  • Deng S, Ke T, Li LT, Cai SW, Zhou YY, Liu Y, Guo LM, Chen LZ, Zhang DY (2017) Impacts of environmental factors on the whole microbial communities in the rhizosphere of a metal-tolerant plant, Elsholtzia haichowensis Sun. Environ Pollut 237:1088–1097

    Article  CAS  Google Scholar 

  • Doronila AI, Maddox LE, Reichman SM, King DJ, Kolev SD, Woodrow IE (2014) Vegetation response of Australian native grass species red grass (Bothriochloa macra (Steudel) ST Blake) and spider grass (Enteropogon acicularis (Lindl.) Lazarides) in saline and arsenic contaminated gold mine tailings: a glasshouse study. Miner Eng 56:61–69

    Article  CAS  Google Scholar 

  • Ettler V, Mihaljevic M, Sebek O, Grygar T (2007) Assessment of single extractions for the determination of mobile forms of metals in highly polluted soils and sediments-analytical and thermodynamic approaches. Anal Chim Acta 602:131–140

    Article  CAS  Google Scholar 

  • Evangelou MW, Bauer U, Ebel M, Schaeffer A (2007) The influence of EDDS and EDTA on the uptake of heavy metals of Cd and Cu from soil with tobacco Nicotiana tabacum. Chemosphere 68(2):345–353

    Article  CAS  Google Scholar 

  • Fliessbach A, Martens R, Reber HH (1994) Soil microbial biomass and microbial activity in soils treated with heavy metal contaminated sewage sludge. Soil Biol Biochem 26(9):1201–1205

    Article  Google Scholar 

  • Gonzaga MIS, Ma LQ, Santos JAG, Matias MIS (2009) Rhizosphere characteristics of two arsenic hyperaccumulating Pteris ferns. Sci Total Environ 407(16):4711–4716

    Article  CAS  Google Scholar 

  • Guarino C, Sciarrillo R (2017) Effectiveness of in situ application of an Integrated Phytoremediation System (IPS) by adding a selected blend of rhizosphere microbes to heavily multi-contaminated soils. Ecol Eng 99:70–82

    Article  Google Scholar 

  • Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177(1–3):437–444

    Article  CAS  Google Scholar 

  • Hu R, Sun K, Su X, Pan YX, Zhang YF, Wang XP (2012) Physiological responses and tolerance mechanisms to Pb in two xerophils, Salsola passerina Bunge and Chenopodium album L. J Hazard Mater 205:131–138

    Article  CAS  Google Scholar 

  • Kim S, Kang H (2011) Effects of elevated CO2 and Pb on phytoextraction and enzyme activity. Water Air Soil Pollut 219(1–4):365–375

    Article  CAS  Google Scholar 

  • Lee SH, Ji W, Lee WS, Koo N, Koh IH, Kim MS, Park JS (2014) Influence of amendments and aided phytostabilization on metal availability and mobility in Pb/Zn mine tailings. J Environ Manag 139:15–21

    Article  CAS  Google Scholar 

  • Li YL, Liu YG, Liu JL, Zeng GM, Li X (2008) Effects of EDTA on lead uptake by Typha orientalis Presl, a new lead-accumulating species in southern China. Bull Environ Contam Toxicol 81(1):36–41

    Article  CAS  Google Scholar 

  • Li TQ, Di ZZ, Islam E, Jiang H, Yang XE (2011) Rhizosphere characteristics of zinc hyperaccumulator Sedum alfredii involved in zinc accumulation. J Hazard Mater 185(2–3):818–823

    Article  CAS  Google Scholar 

  • Li TQ, Tao Q, Han X, Yang XE (2013a) Effects of elevated CO2 on rhizosphere characteristics of Cd/Zn hyperaccumulator Sedum alfredii. Sci Total Environ 454:510–516

    Article  CAS  Google Scholar 

  • Li TQ, Liang CF, Han X, Yang XE (2013b) Mobilization of cadmium by dissolved organic matter in the rhizosphere of hyperaccumulator Sedum alfredii. Chemosphere 91(7):970–976

    Article  CAS  Google Scholar 

  • Lu RK (1999) Analysis of soil agrochemistry. Chinese Agricultural Science and Technology Press, Beijing, pp 1–246 (in Chinese)

    Google Scholar 

  • Lu M, Xu K, Chen J (2013) Effect of pyrene and cadmium on microbial activity and community structure in soil. Chemosphere 91(4):491–497

    Article  CAS  Google Scholar 

  • Luster J, Göttlein A, Nowack B, Sarret G (2009) Sampling, defining, characterising and modelling the rhizosphere - the soils science toolbox. Plant Soil 321:457–482

    Article  CAS  Google Scholar 

  • Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29(2):248–258

    Article  CAS  Google Scholar 

  • Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, Li RH, Zhang ZQ (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicol Environ Saf 126:111–121

    Article  CAS  Google Scholar 

  • Maiz I, Arambarri I, Garcia R, Millan E (2000) Evaluation of heavy metal availability in polluted soils by two sequential extraction procedures using factor analysis. Environ Pollut 110:3–9

    Article  CAS  Google Scholar 

  • Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems, an overview with special reference to phytoremediation. Int J Environ Sci Technol 11(3):843–872

    Article  CAS  Google Scholar 

  • Masciandaro G, Macci C, Peruzzi E, Ceccanti B, Doni S (2013) Organic matter–microorganism–plant in soil bioremediation, a synergic approach. Rev Environ Sci Biotechnol 12(4):399–419

    Article  CAS  Google Scholar 

  • Meeinkuirt W, Kruatrachue M, Tanhan P, Chaiyarat R, Pokethitiyook P (2013) Phytostabilization potential of Pb mine tailings by two grass species, Thysanolaena maxima and Vetiveria zizanioides. Water Air Soil Pollut 224(10):1750

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mendez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments-an emerging remediation technology. Environ Health Perspect 116(3):278–283

    Article  CAS  Google Scholar 

  • Moyé J, Picard-Lesteven T, Zouhri L, El Amari K, Hibti M, Benkaddour A (2017) Groundwater assessment and environmental impact in the abandoned mine of Kettara (Morocco). Environ Pollut 231:899–907

    Article  CAS  Google Scholar 

  • Muszyńska E, Mateusz L, Różańska E, Hanus-Fajerska E, Znojek E (2018) Heavy metal tolerance in contrasting ecotypes of Alyssum montanum. Ecotoxicol Environ Saf 161:305–317

    Article  CAS  Google Scholar 

  • Parelho C, Rodrigues AS, Barreto MC, Ferreira NGC, Garcia P (2016) Assessing microbial activities in metal contaminated agricultural volcanic soils - an integrative approach. Ecotoxicol Environ Saf 129:242–249

    Article  CAS  Google Scholar 

  • Park JH, Lamb D, Paneerselvam P, Choppala G, Bolan N, Chung JW (2011) Role of organic amendments on enhanced bioremediation of heavy metal (loid) contaminated soils. J Hazard Mater 185(2–3):549–574

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Shakoor MB, Ali S, Farid M, Farooq MA, Tauqeer HM, Iftikhar U, Hannan F, Bharwana SA (2013) Heavy metal pollution, a global problem and its remediation by chemically enhanced phytoremediation, a review. J Biol Environ Sci 3:12–20

    Google Scholar 

  • Shu XH, Zhang Q, Lu GN, Yi XY, Dang Z (2017) Pollution characteristics and assessment of sulfide tailings from the Dabaoshan Mine, China. Int Biodeterior Biodegradation 128:122–128

    Article  CAS  Google Scholar 

  • Silva EFD, Durães N, Reis P, Patinha C, Matos J, Costa MR (2015) An integrative assessment of environmental degradation of Caveira abandoned mine area (Southern Portugal). J Geochem Explor 159:33–47

    Article  CAS  Google Scholar 

  • Singh R, Tripathi RD, Dwivedi S, Kumar A, Trivedi PK, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101(9):3025–3032

    Article  CAS  Google Scholar 

  • Tripathy S, Bhattacharyya P, Mohapatra R, Som A, Chowdhury D (2014) Influence of different fractions of heavy metals on microbial ecophysiological indicators and enzyme activities in century old municipal solid waste amended soil. Ecol Eng 70:25–34

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707

    Article  CAS  Google Scholar 

  • Wang YP, Li QB, Shi JY, Lin Q, Chen XC, Wu WX, Chen YX (2008) Assessment of microbial activity and bacterial community composition in the rhizosphere of a copper accumulator and a non-accumulator. Soil Biol Biochem 40:1167–1177

    Article  CAS  Google Scholar 

  • Wei S, Twardowska I (2013) Main rhizosphere characteristics of the Cd hyperaccumulator Rorippa globosa (Turcz.) Thell. Plant Soil 372(1–2):669–681

    Article  CAS  Google Scholar 

  • Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321:385–408

    Article  CAS  Google Scholar 

  • Wójcik M, Tukiendorf A (2014) Accumulation and tolerance of lead in two contrasting ecotypes of Dianthus carthusianorum. Phytochemistry 100:60–65

    Article  CAS  Google Scholar 

  • Yang B, Zhou M, Zhou LL, Xue ND, Zhang SL, Lan CY (2015) Variability of cadmium, lead, and zinc tolerance and accumulation among and between germplasms of the fiber crop Boehmeria nivea with different root-types. Environ Sci Pollut Res 22(18):13960–13969

    Article  CAS  Google Scholar 

  • Zhan J, Li TX, Yu HY, Zhang XZ, Zhao L (2016) The influence of humic substance on Cd accumulation of phytostabilizer Athyrium wardii (Hook.) grown in Cd-contaminated soils. Environ Sci Pollut Res 23(18):18524–18532

    Article  CAS  Google Scholar 

  • Zhan J, Li TX, Zhang XZ, Yu HY, Zhao L (2018) Rhizosphere characteristics of phytostabilizer Athyrium wardii (Hook.) involved in Cd and Pb accumulation. Ecotoxicol Environ Saf 148:892–900

    Article  CAS  Google Scholar 

  • Zhang SJ, Li TX, Huang HG, Zou TJ, Zhang XZ, Yu HY, Zheng ZC, Wang YD (2012) Cd accumulation and phytostabilization potential of dominant plants surrounding mining tailings. Environ Sci Pollut Res 19(9):3879–3888

    Article  CAS  Google Scholar 

  • Zhang SJ, Li TX, Zhang XZ, Yu HY, Zheng ZC, Wang YD, Hao XQ, Pu Y (2014) Changes in pH, dissolved organic matter and Cd species in the rhizosphere soils of Cd phytostabilizer Athyrium wardii (Hook.) Makino involved in Cd tolerance and accumulation. Environ Sci Pollut Res 21:4605–4613

    Article  CAS  Google Scholar 

  • Zhao L, Li TX, Yu HY, Chen GD, Zhang XZ, Zheng ZC, Li JX (2015) Changes in chemical forms, subcellular distribution, and thiol compounds involved in Pb accumulation and detoxification in Athyrium wardii (Hook.). Environ Sci Pollut Res 22(16):12676–12688

    Article  CAS  Google Scholar 

  • Zhao L, Li TX, Zhang XZ, Chen GD, Zheng ZC, Yu HY (2016a) Pb uptake and phytostabilization potential of the mining ecotype of Athyrium wardii (Hook.) grown in Pb-contaminated Soil. Clean Soil Air Water 44(9):1184–1190

    Article  CAS  Google Scholar 

  • Zhao L, Li TX, Zhang XZ, Chen GD, Zheng ZC, Yu HY (2016b) Rhizosphere characteristics of Pb phytostabilizer Athyrium wardii (Hook.) involved in Pb accumulation. Environ Earth Sci 75(6):463

    Article  CAS  Google Scholar 

  • Zhou HM, Zhang DX, Wang P, Liu XY, Cheng K, Li LQ, Zheng JW, Zhang XH, Zheng JF, Crowley G, Zwieten L, Pan G (2017) Changes in microbial biomass and metabolic quotient with biochar addition to agricultural soils: a meta-analysis. Agric Ecosyst Environ 239:80–89

    Article  CAS  Google Scholar 

  • Zhu GX, Xiao HY, Guo QJ, Song B, Zheng GD, Zhang ZY, Zhao JJ, Okoli CP (2018) Heavy metal contents and enrichment characteristics of dominant plants in wasteland of the downstream of a lead-zinc mining area in Guangxi, Southwest China. Ecotoxicol Environ Saf 151:266–271

    Article  CAS  Google Scholar 

  • Zou TJ, Li TX, Zhang XZ, Yu HY, Luo HB (2011) Lead accumulation and tolerance characteristics of Athyrium wardii (Hook.) as a potential phytostabilizer. J Hazard Mater 186(1):683–689

    Article  CAS  Google Scholar 

  • Zou TJ, Li TX, Zhang XZ, Yu HY, Huang HG (2012) Lead accumulation and phytostabilization potential of dominant plant species growing in a lead–zinc mine tailing. Environ Earth Sci 65(3):621–630

    Article  CAS  Google Scholar 

Download references

Funding

This study was financially supported by the National Key Research and Development Program (2018YFD0800600) and Sichuan Key Research Programs (2017SZ0188, 2017SZ0198, and 2018SZ0326).

Author information

Authors and Affiliations

  1. College of Resources, Sichuan Agricultural University, 211 Huimin Road, Chengdu, 611130, Sichuan, China

    Qingpei Zhang, Juan Zhan, Haiying Yu, Tingxuan Li, Xizhou Zhang, Huagang Huang & Yunhong Zhang

Authors
  1. Qingpei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Zhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haiying Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tingxuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xizhou Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Huagang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yunhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haiying Yu.

Additional information

Responsible editor: Elena Maestri

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Qingpei Zhang and Juan Zhan are the co-first authors.

Electronic supplementary material

ESM 1

(DOC 60 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Q., Zhan, J., Yu, H. et al. Lead accumulation and soil microbial activity in the rhizosphere of the mining and non-mining ecotypes of Athyrium wardii (Hook.) Makino in adaptation to lead-contaminated soils. Environ Sci Pollut Res 26, 32957–32966 (2019). https://doi.org/10.1007/s11356-019-06395-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06395-1

Keywords

Search

Navigation