Compounded chelating agent derived from fruit residue extracts effectively enhances Cd phytoextraction by Sedum alfredii

Highlights

• Cd extractability of eleven kinds of fruit residue extractions was compared.

• The most effective volume ratio of LRE, GLDA and tea saponin in Cd phytoextraction was 15:4:1.

• CPC improved plant growth, Cd phytoextraction performance and soil organic matter content.

• CPC induced less changes in bacterial community composition and had no evident influence on MBC and bacterial α-diversity.

Abstract

A chelating agent is known as the enhancer for metal phytoextraction; however, there is still a lack of efficient and environmentally sustainable chelators. Here, lemon residue extraction (LRE), prepared from 11 kinds of fruit wastes, was combined with N, N-bis (carboxymethyl) glutamic acid (GLDA), and tea saponin (T.S.) for the compounded plant-derived chelator (CPC), and their influences on Cd phytoextraction by the hyperaccumulator Sedum alfredii was evaluated. Among these fruits, the lemon residue extracted the most significant amount of Cd from the soil. The most effective CPC was at the volume ratio of three agents being 15:4:1 (LRE: GLDA: T.S.). Compared with the deionized water, the solubility of three Cd minerals was increased by 36~311 times, and Cd speciation was substantially altered after CPC application. In the pot experiment, CPC addition caused evident increases in plant shoot biomass, Cd phytoextraction efficiency, and organic matter content compared with EDTA and nitrilotriacetic acid (NTA) application. CPC induced fewer changes in bacterial community composition compared with EDTA and had no pronounced influence on microbial biomass carbon and bacterial α-diversity, suggesting CPC had a subtle impact on the microbiological environments. Our study provides a theoretical base for the reutilization of fruit wastes and the development of environmental-friendly chelator that assists Cd phytoextraction.

Graphical abstract

Keywords

Compounded plant-derived chelator / Fruit residue / Cadmium / Phytoextraction / Sedum alfredii

References

[1] Abou-Shanab, R., Angle, J., Chaney, R., 2006. Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biology & Biochemistry 38, 2882–2889

[2] Anwar, S., Khan, S., Ashraf, M.Y., Noman, A., Zafar, S., Liu, L., Ullah, S., Fahad, S., 2017. Impact of chelator-induced phytoextraction of Cd on yield and ionic uptake of maize. International Journal of Phytoremediation 19, 505–513

[3] Banat, K.M., Howari, F.M., Al-Hamad, A.A., 2005. Heavy metals in urban soils of central Jordan: Should we worry about their environmental risks? Environmental Research 97, 258–273

[4] Barrutia, O., Garbisu, C., Hernández-Allica, J., García-Plazaola, J.I., Becerril, J.M., 2010. Differences in EDTA-assisted metal phytoextraction between metallicolous and non-metallicolous accessions of Rumex acetosa L. Environmental Pollution 158, 1710–1715

[5] Buekens, A., Huang, H., 1998. Comparative evaluation of techniques for controlling the formation and emission of chlorinated dioxins furans in municipal waste incineration. Journal of Hazardous Materials 62, 1–33

[6] Cai, Y., Hu, K., Zheng, Z., Zhang, Y., Guo, S., Zhao, X., Cui, Z., Wang, X., 2019. Effects of adding EDTA and Fe²⁺ on the performance of reactor and microbial community structure in two simulated phases of anaerobic digestion. Bioresource Technology 275, 183–191

[7] Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583

[8] Cay, S., 2016. Enhancement of Cd uptake by Amaranthus caudatus, an ornamental plant, using tea saponin. Environmental Monitoring and Assessment 188, 320

[9] Chen, Y., Hu, L., Liu, X., Deng, Y., Liu, M., Xu, B., Wang, M., Wang, G., 2017. Influences of king grass (Pennisetum sinese Roxb)-enhanced approaches for phytoextraction and microbial communities in multi-metal contaminated soil. Geoderma 307, 253–266

[10] Deng, G., Shen, C., Xu, X., Kuang, R., Guo, Y., Zeng, L., Gao, L., Lin, X., Xie, J., Xia, E., Li, S., Wu, S., Chen, F., Ling, W., Li, H., 2012. Potential of fruit wastes as natural resources of bioactive compounds. International Journal of Molecular Sciences 13, 8308–8323

[11] Duquène, L., Vandenhove, H., Tack, F., Meers, E., Baeten, J., Wannijn, J., 2009. Enhanced phytoextraction of uranium and selected heavy metals by Indian mustard and ryegrass using biodegradable soil amendments. Science of the Total Environment 407, 1496–1505

[12] Ehsan, S., Ali, S., Noureen, S., Mahmood, K., Farid, M., Ishaque, W., Shakoor, M.B., Rizwan, M., 2014. Citric acid assisted phytoremediation of Cd by Brassica napus L. Ecotoxicology and Environmental Safety 106, 164–172

[13] Fierer, N., Bradford, M.A., Jackson, R.B., 2007. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364

[14] Gao, Y., Miao, C., Mao, L., Zhou, P., Jin, Z., Shi, W., 2010. Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. Journal of Hazardous Materials 181, 771–777

[15] González-Molina, E., Domínguez-Perles, R., Moreno, D.A., García-Viguera, C., 2010. Natural bioactive compounds of Ctrus limon for food and health. Journal of Pharmaceutical and Biomedical Analysis 51, 327–345

[16] Grčman, H., Velikonja-Bolta, Š., Vodnik, D., Kos, B., Leštan, D., 2001. EDTA enhanced heavy metal phytoextraction: metal accumulation, leaching and toxicity. Plant and Soil 235, 105–114

[17] Guo, X., Luo, J., Du, Y., Li, J., Liu, Y., Liang, Y., Li, T., 2021. Coordination between root cell wall thickening and pectin modification is involved in cadmium accumulation in Sedum alfredii. Environmental Pollution 268, 115665

[18] Guo, X., Zhang, G., Wei, Z., Zhang, L., He, Q., Wu, Q., Qian, T., 2018. Mixed chelators of EDTA, GLDA, and citric acid as washing agent effectively remove Cd, Zn, Pb, and Cu from soils. Journal of Soils and Sediments 18, 835–844

[19] Hassan, M., Sighicelli, M., Lai, A., Colao, F., Ahmed, A.H.H., Fantoni, R., Harith, M.A., 2008. Studying the enhanced phytoremediation of lead contaminated soils via laser induced breakdown spectroscopy. Spectrochimica Acta. Part B, Atomic Spectroscopy 63, 1225–1229

[20] Hseu, Z., Jien, S., Wang, S., Deng, H., 2013. Using EDDS and NTA for enhanced phytoextraction of Cd by water spinach. Journal of Environmental Management 117, 58–64

[21] Hu, X., Liu, X., Zhang, X., Cao, L., Chen, J., Yu, H., 2017. Increased accumulation of Pb and Cd from contaminated soil with Scirpus triqueter by the combined application of NTA and APG. Chemosphere 188, 397–402

[22] Hunter, M., Stephenson, T., Kirk, P.W., Perry, R., Lester, J.N., 1986. Effect of salinity gradients and heterotrophic microbial activity on biodegradation of nitrilotriacetic acid in laboratory simulations of the estuarine environment. Applied and Environmental Microbiology 51, 919–925

[23] Jiang, H., Li, T., Han, X., Yang, X., He, Z., 2012. Effects of pH and low molecular weight organic acids on competitive adsorption and desorption of cadmium and lead in paddy soils. Environmental Monitoring and Assessment 184, 6325–6335

[24] Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., Gloeckner, F.O., 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research 41, e1

[25] Kołodyńska, D., 2011. Cu(II), Zn(II), Co(II) and Pb(II) removal in the presence of the complexing agent of a new generation. Desalination 267, 175–183

[26] Leštan, D., Luo, C., Li, X., 2008. The use of chelating agents in the remediation of metal-contaminated soils: A review. Environmental Pollution 153, 3–13

[27] Li, J., Lu, Y., Shim, H., Deng, X., Lian, J., Jia, Z., Li, J., 2010a. Use of the BCR sequential extraction procedure for the study of metal availability to plants. Journal of Environmental Monitoring 12, 466–471

[28] Li, W.C., Ye, Z.H., Wong, M.H., 2010b. Metal mobilization and production of short-chain organic acids by rhizosphere bacteria associated with a Cd/Zn hyperaccumulating plant, Sedum alfredii. Plant and Soil 326, 453–467

[29] Li, Y., Liu, K., Wang, Y., Zhou, Z., Chen, C., Ye, P., Yu, F., 2018. Improvement of Cd phytoremediation by Centella asiatica L. after soil inoculation with Cd-resistant Enterobacter sp. FM-1. Chemosphere 202, 280–288

[30] Li, Z., Jia, M., Wu, L., Christie, P., Luo, Y., 2016. Changes in metal availability, desorption kinetics and speciation in contaminated soils during repeated phytoextraction with the Zn/Cd hyperaccumulator Sedum plumbizincicola. Environmental Pollution 209, 123–131

[31] Liu, D., Islam, E., Li, T., Yang, X., Jin, X., Mahmood, Q., 2008. Comparison of synthetic chelators and low molecular weight organic acids in enhancing phytoextraction of heavy metals by two ecotypes of Sedum alfredii Hance. Journal of Hazardous Materials 153, 114–122

[32] Liu, D., Li, T., Yang, X., Islam, E., Jin, X., Mahmood, Q., 2007. Enhancement of lead uptake by hyperaccumulator plant species Sedum alfredii Hance using EDTA and IAA. Bulletin of Environmental Contamination and Toxicology 78, 280–283

[33] Liu, X., Cao, L., Wang, Q., Zhang, X., Hu, X., 2017. Effect of tea saponin on phytoremediation of Cd and pyrene in contaminated soils by Lolium multiflorum. Environmental Science and Pollution Research International 24, 18946–18952

[34] Luo, C.L., Shen, Z.G., Li, X.D., 2005. Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59, 1–11

[35] Luo, J., Tao, Q., Wu, K., Li, J., Qian, J., Liang, Y., Yang, X., Li, T., 2017. Structural and functional variability in root-associated bacterial microbiomes of Cd/Zn hyperaccumulator Sedum alfredii. Applied Microbiology and Biotechnology 101, 7961–7976

[36] Luo, Y.M., Christie, P., 1998. Choice of extraction technique for soil reducible trace metals determines the subsequent oxidisable metal fraction in sequential extraction schemes. International Journal of Environmental Analytical Chemistry 72, 59–75

[37] Lux, A., Martinka, M., Vaculik, M., White, P.J., 2010. Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany 62, 21–37

[38] Mahar, A., Wang, P., Ali, A., Awasthi, M.K., Lahori, A.H., Wang, Q., Li, R., Zhang, Z., 2016. Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: A review. Ecotoxicology and Environmental Safety 126, 111–121

[39] Meng, F., Yuan, G., Wei, J., Bi, D., Ok, Y.S., Wang, H., 2017. Humic substances as a washing agent for Cd-contaminated soils. Chemosphere 181, 461–467

[40] Moćko, A., Wacławek, W., 2004. Three-step extraction procedure for determination of heavy metals availability to vegetables. Analytical and Bioanalytical Chemistry 380, 813–817

[41] Ning, Y., Liu, N., Song, Y., Luo, J., Li, T., 2019. Enhancement of phytoextraction of Pb by compounded activation agent derived from fruit residue. International Journal of Phytoremediation 21, 1449–1456

[42] Nour, V., Trandafir, I., Elena, I.M., 2010. HPLC organic acid analysis in different citrus juices under reversed phase conditions. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 38, 44–48.

[43] Nowack, B., Schulin, R., Robinson, B.H., 2006. Critical assessment of chelant-enhanced metal phytoextraction. Environmental Science & Technology 40, 5225–5232

[44] Pavloušek, P., Kumšta, M., 2011. Profiling of primary metabolites in grapes of interspecific grapevine varieties: sugars and organic acids. Czech Journal of Food Sciences 29, 361–372

[45] Penniston, K.L., Nakada, S.Y., Holmes, R.P., Assimos, D.G., 2008. Quantitative assessment of citric acid in lemon juice, lime juice, and commercially-available fruit juice products. Journal of Endourology 22, 567–570

[46] Philip, D., 2003. VEGAN, a package of R functions for community ecology. Journal of Vegetation Science 14, 927–930

[47] Sabir, M., Hanafi, M.M., Zia-Ur-Rehman, M., Saifullah, , Ahmad, H.R., Hakeem, K.R., AzizT., 2014. Comparison of low-molecular-weight organic acids and ethylenediaminetetraacetic acid to enhance phytoextraction of heavy metals by maize. Communications in Soil Science and Plant Analysis 45, 42–52

[48] Sessitsch, A., Kuffner, M., Kidd, P., Vangronsveld, J., Wenzel, W.W., Fallmann, K., Puschenreiter, M., 2013. The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biology & Biochemistry 60, 182–194

[49] Shoran, V., Shoran, A.S., Poonia, P., 2016. Factors affecting phytoextraction: a review. Pedosphere 26, 148-166.

[50] Tandy, S., Schulin, R., Nowack, B., 2006. Uptake of metals during chelant-assisted phytoextraction with EDDS related to the solubilized metal concentration. Environmental Science & Technology 40, 2753–2758

[51] Tang, S., Bai, J., Yin, H., Ye, J., Peng, H., Liu, Z., Dang, Z., 2014. Tea saponin enhanced biodegradation of decabromodiphenyl ether by Brevibacillus brevis. Chemosphere 114, 255–261

[52] Vassil, A.D., Kapulnik, Y., Raskin, I.I., Salt, D.E., 1998. The role of EDTA in lead transport and accumulation by indian mustard. Plant Physiology 117, 447–453

[53] Vivas, A., Biró, B., Ruíz-Lozano, J.M., Barea, J.M., Azcón, R., 2006. Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 62, 1523–1533

[54] Wang, G., Zhang, S., Xu, X., Zhong, Q., Zhang, C., Jia, Y., Li, T., Deng, O., Li, Y., 2016. Heavy metal removal by GLDA washing: optimization, redistribution, recycling, and changes in soil fertility. Science of the Total Environment 569–570, 557–568

[55] Wu, Q., Cui, Y., Li, Q., Sun, J., 2015. Effective removal of heavy metals from industrial sludge with the aid of a biodegradable chelating ligand GLDA. Journal of Hazardous Materials 283, 748–754

[56] Wu, Q.T., Wei, Z.B., Ouyang, Y., 2007. Phytoextraction of metal-contaminated soil by Sedum alfredii H: effects of chelator and co-planting. Water, Air, and Soil Pollution 180, 131–139

[57] Xia, H.L., Chi, X.Y., Yan, Z.J., Cheng, W.W., 2009. Enhancing plant uptake of polychlorinated biphenyls and Cd using tea saponin. Bioresource Technology 100, 4649–4653

[58] Yang, J.Y., Yang, X.E., He, Z.L., Li, T.Q., Shentu, J.L., Stoffella, P.J., 2006. Effects of pH, organic acids, and inorganic ions on lead desorption from soils. Environmental Pollution 143, 9–15

[59] Yang, L., Luo, C., Liu, Y., Quan, L., Chen, Y., Shen, Z., 2013. Residual effects of EDDS leachates on plants during EDDS-assisted phytoremediation of copper contaminated soil. Science of the Total Environment 444, 263–270

[60] Yang, X.E., Long, X.X., Ye, H.B., He, Z.L., Calvert, D.V., Stoffella, P.J., 2004. Cd tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant and Soil 259, 181–189

[61] Ye, M., Sun, M., Wan, J., Fang, G., Li, H., Hu, F., Jiang, X., Orori Kengara, F., 2015. Evaluation of enhanced soil washing process with tea saponin in a peanut oil-water solvent system for the extraction of PBDEs/PCBs/PAHs and heavy metals from an electronic waste site followed by vetiver grass phytoremediation. Journal of Chemical Technology and Biotechnology (Oxford, Oxfordshire) 90, 2027–2035

[62] Yu, X., He, Y., 2018. Tea saponins: effective natural surfactants beneficial for soil remediation, from preparation to application. RSC Advances 8, 24312–24321

[63] Zhao, Z., Xi, M., Jiang, G., Liu, X., Bai, Z., Huang, Y., 2010. Effects of IDSA, EDDS and EDTA on heavy metals accumulation in hydroponically grown maize (Zea mays L.). Journal of Hazardous Materials 181, 455–459

Acknowledgments

This research was financially supported by the National Natural Science Foundation of China (41671315,41977107), National Postdoctoral Program for Innovative Talents (BX20200293), Zhejiang Provincial Natural Science Foundation of China (LZ18D010001), National Key Research and Development Project of China (2016YFD0800802), and the Fundamental Research Funds for the Central Universities, China's Agriculture Research System (CARS-04), and Fundamental Research Funds for the Central Universities (2020FZZX001-06).

RIGHTS & PERMISSIONS

2021 Higher Education Press