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.
Similar content being viewed by others
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
Barros N, Gallego M, Feijóo S (2007) Sensitivity of calorimetric indicators of soil microbial activity. Thermochim Acta 458:18–22
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
Egli T (2001) Biodegradation of metal-complexing aminopolycarboxylic acids. J Biosci Bioeng 92:89–97
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
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
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
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
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
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
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
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
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
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
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
Lu RK (2000) Analysis methods of soil agricultural chemistry. China Agricultural Science Press, Beijing (in Chinese)
Luo CL, Shen ZG, Li XD (2005) Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59:1–11
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
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
Madsen EL (2011) Microorganisms and their roles in fundamental biogeochemical cycles. Current Opinion Biotechnol 22:456–464
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
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
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
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
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
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
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
Saifullah ME, Qadir M, de Caritat P, Tack FMG, Du LG, Zia MH (2009) EDTA-assisted Pb phytoextraction. Chemosphere 74:1279–1291
Sparling GP (1981) Heat output of the soil biomass. Soil Biol Biochem 13:373–376
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
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
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
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
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
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
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
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
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
Acknowledgements
This research was financially supported by the National Natural Science Foundation of China (41571314, 41201226).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Zhihong Xu
Electronic supplementary material
ESM 1
(DOCX 215 kb).
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-9029-y