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Deciphering biodegradable chelant-enhanced phytoremediation through microbes and nitrogen transformation in contaminated soils

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Abstract

Biodegradable chelant-enhanced phytoremediation offers an alternative treatment technique for metal contaminated soils, but most studies to date have addressed on phytoextraction efficiency rather than comprehensive understanding of the interactions among plant, soil microbes, and biodegradable chelants. In the present study, we investigated the impacts of biodegradable chelants, including nitrilotriacetate, S,S-ethylenediaminedisuccinic acid (EDDS), and citric acid on soil microbes, nitrogen transformation, and metal removal from contaminated soils. The EDDS addition to soil showed the strongest ability to promote the nitrogen cycling in soil, ryegrass tissue, and microbial metabolism in comparison with other chelants. Both bacterial community-level physiological profiles and soil mass specific heat rates demonstrated that soil microbial activity was inhibited after the EDDS application (between day 2 and 10), but this effect completely vanished on day 30, indicating the revitalization of microbial activity and community structure in the soil system. The results of quantitative real-time PCR revealed that the EDDS application stimulated denitrification in soil by increasing nitrite reductase genes, especially nirS. These new findings demonstrated that the nitrogen release capacity of biodegradable chelants plays an important role in accelerating nitrogen transformation, enhancing soil microbial structure and activity, and improving phytoextraction efficiency in contaminated soil.

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References

  • Barros N, Feijóo S, Fernández S (2003) Microcalorimetric determination of the cell specific heat rate in soils: relationship with the soil microbial population and biophysic significance. Thermochim Acta 406:161–170

    Article  CAS  Google Scholar 

  • Barros N, Gallego M, Feijóo S (2007) Sensitivity of calorimetric indicators of soil microbial activity. Thermochim Acta 458:18–22

    Article  CAS  Google Scholar 

  • Cheng GL, Ma XF, Sun XB, Zhao SQ (2012) Effects of EDTA, EDDS and citric acid on growth of maize and uptake of lead by maize in contaminated soil. Adv Res Mater Sci Environ Sci 534:277–280

    CAS  Google Scholar 

  • Egli T (2001) Biodegradation of metal-complexing aminopolycarboxylic acids. J Biosci Bioeng 92:89–97

    Article  CAS  Google Scholar 

  • Epelde L, Hernandez-Allica J, Becerril JM, Blanco F, Garbisu C (2008) Effects of chelates on plants and soil microbial community: comparison of EDTA and EDDS for lead phytoextraction. Sci Total Environ 401:21–28

    Article  CAS  Google Scholar 

  • Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359

    CAS  Google Scholar 

  • Giansoldati V, Tassi E, Morelli E, Gabellieri E, Pedron F, Barbafieri M (2012) Nitrogen fertilizer improves boron phytoextraction by Brassica juncea grown in contaminated sediments and alleviates plant stress. Chemosphere 87:1119–1125

    Article  CAS  Google Scholar 

  • Hernandez-Allica J, Garbisu C, Barrutia O, Becerril JM (2007) EDTA-induced heavy metal accumulation and phytotoxicity in cardoon plants. Environ Experimen Bot 60:26–32

    Article  CAS  Google Scholar 

  • Kaiser EA, Mueller T, Joergensen RG, Insam H, Heinemeyer O (1992) Evaluation of methods to estimate the soil microbial biomass and the relationship with soil texture and organic-matter. Soil Biol Biochem 24:675–683

    Article  CAS  Google Scholar 

  • Kayser A, Wenger K, Keller A, Attinger W, Felix HR, Gupta SK, Schulin R (2000) Enhancement of phytoextraction of Zn, cd, and cu from calcareous soil: the use of NTA and sulfur amendments. Environ Sci Technol 34:1778–1183

    Article  CAS  Google Scholar 

  • Kos B, Lestan D (2003) Influence of a biodegradable ([S,S]-EDDS) and nondegradable (EDTA) chelate and hydrogel modified soil water sorption capacity on Pb phytoextraction and leaching. Plant Soil 253:403–411

    Article  CAS  Google Scholar 

  • Leštan D, Luo CL, Li XD (2008) The use of chelating agents in the remediation of metal-contaminated soils: a review. Environ Pollut 153:3–13

    Article  Google Scholar 

  • Li XD, Poon CS, Liu PS (2001) Concentration and chemical partitioning of road dusts and urban soils in Hong Kong. Appl Geochem 16:1361–1368

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) methods. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Loosemore N, Straczek A, Hinsinger P, Jaillard B (2004) Zinc mobilization from a contaminated soil by three genotypes of tobacco as affected by soil and rhizosphere pH. Plant Soil 260:19–32

    Article  CAS  Google Scholar 

  • Lu RK (2000) Analysis methods of soil agricultural chemistry. China Agricultural Science Press, Beijing (in Chinese)

    Google Scholar 

  • Luo CL, Shen ZG, Li XD (2005) Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59:1–11

    Article  CAS  Google Scholar 

  • Luo CL, Shen ZG, Lou LQ, Li XD (2006) EDDS and EDTA-enhanced phytoextraction of metals from artificially contaminated soil and residual effects of chelant compounds. Environ Pollut 144:862–871

    Article  CAS  Google Scholar 

  • Luo CL, Wang SR, Wang Y, Yang RX, Zhang G (2015) Effects of EDDS and plant-growth-promoting bacteria on plant uptake of trace metals and PCBs from e-waste-contaminated soil. J Hazard Mater 286:379–385

    Article  CAS  Google Scholar 

  • Madsen EL (2011) Microorganisms and their roles in fundamental biogeochemical cycles. Current Opinion Biotechnol 22:456–464

    Article  CAS  Google Scholar 

  • Meers E, Tack FMG, Verloo MG (2008) Degradability of ethylenediaminedisuccinic acid (EDDS) in metal contaminated soils—implications for its use soil remediation. Chemosphere 70:358–363

    Article  CAS  Google Scholar 

  • Mueller KE, Hobbie SE, Tilman D, Reich PB (2013) Effects of plant diversity, N fertilization, and elevated carbon dioxide on grassland soil N cycling in a long-term experiment. Glob Chang Biol 19:1249–1261

    Article  Google Scholar 

  • Muhlbachova G (2011) Soil microbial activities and heavy metal mobility in long-term contaminated soils after addition of EDTA and EDDS. Ecol Eng 37:1064–1071

    Article  Google Scholar 

  • Philippot L, Čuhel J, Saby NPA, Chèneby D, Chroňáková A, Bru D, Arrouays D, Martin-Laurent F, Simek M (2009) Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ Microbiol 11:1518–1526

    Article  Google Scholar 

  • Prieto C, Lozano JC, Rodriguez PB, Tome FV (2013) Enhancing radium solubilization in soils by citrate, EDTA, and EDDS chelating amendments. J Hazard Mater 250:439–446

    Article  Google Scholar 

  • Quartacci MF, Irtelli B, Baker AJ, Navari-Izzo F (2007) The use of NTA and EDDS for enhanced phytoextraction of metals from a multiply contaminated soil by Brassica carinata. Chemosphere 68:1920–1928

    Article  CAS  Google Scholar 

  • Rodrigues DF, Tiedje JM (2007) Multi-locus real-time PCR for quantitation of bacteria in the environment reveals Exiguobacterium to be prevalent in permafrost. FEMS Microbiol Ecol 59:489–499

    Article  CAS  Google Scholar 

  • Saifullah ME, Qadir M, de Caritat P, Tack FMG, Du LG, Zia MH (2009) EDTA-assisted Pb phytoextraction. Chemosphere 74:1279–1291

    Article  CAS  Google Scholar 

  • Sparling GP (1981) Heat output of the soil biomass. Soil Biol Biochem 13:373–376

    Article  CAS  Google Scholar 

  • Ultra VU, Yano A, Iwasaki K, Tanaka S, Kang YM, Sakurai K (2005) Influence of chelating agent addition on copper distribution and microbial activity in soil and copper uptake by brown mustard (Brassica juncea). Soil Sci Plant Nutri 51:193–202

    Article  CAS  Google Scholar 

  • Wang F, Yao J, Chen HL, Zhou Y, Chen YJ, Chen H, Gai N, Zhuang RS, Tian L, Maskow T, Ceccanti B, Trebse P, Zaray G (2009) Microcalorimetric measurements of the microbial activities of single- and mixed-species with trivalent iron in soil. Ecotoxicol Environ Saf 72:128–135

    Article  CAS  Google Scholar 

  • Xie HL, Jiang RF, Zhang FS, McGrath SP, Zhao FJ (2009) Effect of nitrogen form on the rhizosphere dynamics and uptake of cadmium and zinc by the hyperaccumulator Thlaspi caerulescens. Plant Soil 318:205–215

    Article  CAS  Google Scholar 

  • Xue D, Yao HY, Ge DY, Huang CY (2008) Soil microbial community structure in diverse land use systems: a comparative study using Biolog, DGGE, and PLFA analyses. Pedosphere 18:653–663

    Article  CAS  Google Scholar 

  • Yang YG, Campbell CD, Clark L, Cameron CM, Paterson E (2006) Microbial indicators of heavy metal contamination in urban and rural soils. Chemosphere 63:1942–1952

    Article  CAS  Google Scholar 

  • Yang L, Wang GP, Cheng ZN, Liu Y, Shen ZG, Luo CL (2013) Influence of the application of chelant EDDS on soil enzymatic activity and microbial community structure. J Hazard Mater 262:561–570

    Article  CAS  Google Scholar 

  • Yuan Q, Liu PF, Lu YH (2012) Differential responses of nirK- and nirS-carrying bacteria to denitrifying conditions in the anoxic rice field soil. Environ Microb Rep 4:113–122

    Article  CAS  Google Scholar 

  • Zaccheo P, Crippa L, Pasta VDMP (2006) Ammonium nutrition as a strategy for cadmium mobilization in the rhizosphere of sunflower. Plant Soil 283:43–56

    Article  CAS  Google Scholar 

  • Zhao MX, Xue K, Wang F, Liu SS, Bai SJ, Sun B, Zhou JZ, Yang YF (2014) Microbial mediation of biogeochemical cyclings revealed by simulation of global changes with soil transplant and cropping. ISME J 8:2045–2055

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the National Natural Science Foundation of China (41571314, 41201226).

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Authors and Affiliations

  1. State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, 712100, China

    Linchuan Fang

  2. College of Natural Resources and Environment, Northwest A&F University, Yangling, 712100, China

    Mengke Wang

  3. Environmental Biotechnology Laboratory, Department of Civil Engineering, The University of Hong Kong, Hong Kong, China

    Lin Cai

  4. Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Long Cang

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  1. Linchuan Fang
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  2. Mengke Wang
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  3. Lin Cai
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  4. Long Cang
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Correspondence to Long Cang.

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Responsible editor: Zhihong Xu

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Fang, L., Wang, M., Cai, L. et al. Deciphering biodegradable chelant-enhanced phytoremediation through microbes and nitrogen transformation in contaminated soils. Environ Sci Pollut Res 24, 14627–14636 (2017). https://doi.org/10.1007/s11356-017-9029-y

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  • DOI: https://doi.org/10.1007/s11356-017-9029-y

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