Abstract
Poly-γ-glutamic acid (γ-PGA) can be used as a chemical stabilizer to chelate heavy metals in polluted soils. We investigated the effects of γ-PGA on cucumber seedlings under Cd and Pb stresses. γ-PGA effectively reduced the growth inhibitory effects of Cd and Pb on cucumber seedlings. Cd and Pb absorption in cucumber seedlings was also decreased. Further, γ-PGA decreased the malondialdehyde content, and increased the proline content and the total antioxidant capacity of cucumber seedlings in a dose-dependent manner. Infrared spectral characterization of γ-PGA-Cd and γ-PGA-Pb showed that Cd2+ and Pb2+ bind to free carboxyl groups on γ-PGA. Furthermore, γ-PGA-Cd and γ-PGA-Pb were degraded by 22.02 and 24.68%, respectively, within 28 weeks. The chelating rate of γ-PGA-Pb and γ-PGA-Cd reached 27.26 and 14.28%, respectively. Further, γ-PGA alleviated the negative effects of Cd and Pb on soil microorganisms. Thus, γ-PGA can effectively reduce the accumulation of heavy metals in crops caused by heavy metal pollution of farmland, and has significant application value.
Similar content being viewed by others
References
Ahmed A, Tajmir-Riahi HA (1993) Interaction of toxic metal ions Cd2+, Hg2+, and Pb2+ with light-harvesting proteins of chloroplast thylakoid membranes. An FTIR spectroscopic study. J Inorg Biochem 50:235–243
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Boeddi B, Oravecz AR, Lehoczki E (1995) Effect of cadmium on organization and photoreduction of protochlorphyllide in dark-grown leaves and etioplast inner membrane preparations of wheat. Photosynthetica 31:411–420
Boon N, Marlé C, Top EM, Verstraete W (2000) Comparison of the spatial homogeneity of physico-chemical parameters and bacterial 16S rRNA genes in sediment samples from a dumping site for dredging sludge. Appl Microbiol Biot 53:742–747
Casella S, Frassinetti S, Lupi F, Squartini A (1988) Effect of cadmium, chromium and copper on symbiotic and free-living Rhizobium leguminosarum biovar trifolii. FEMS Microbiol Lett 49:343–347
Cocolin L, Aggio D, Manzano M, Cantoni C, Comi G (2002) An application of PCR-DGGE analysis to profile the yeast populations in raw milk. Int Dairy J 12:407–411
Cunningham SD, Berti WR, Huang JW (1995) Phytoremediation of contaminated soils. Trends Biotechnol 13:393–397
El-Tarabily KA, Hardy GESJ, Sivasithamparam K, Kurtböke ID (1996) Microbiological differences between limed and unlimed soils and their relationship with cavity spot disease of carrots (Daucus carota L.) caused by Pythium coloratum in Western Australia. Plant Soil 183:279–290
Evangelou MWH (2007) Biochelators as an alternative to EDTA and other synthetic chelators for the phytoextraction of heavy metals (Cu, Cd, Pb) from soil. Rwth Aachen
Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Cell Mol Life Sci Cmls 46:834–840
Guo Z, Yang N, Zhu C, Gan L (2017) Exogenously applied poly-γ-glutamic acid alleviates salt stress in wheat seedlings by modulating ion balance and the antioxidant system. Environ Sci Pollut R, 1–7
Hikichi K, Tanaka H, Konno A (1990) Nuclear magnetic resonance study of poly(γ-glutamic acid)-Cu(II) and Mn(II) complexes. Polym J 22:103–109
Ho YS, Mckay G (2003) Sorption of dyes and copper ions onto biosorbents. Process Biochem 38:1047–1061
Ho GH, Ho TI, Hsieh KH, Su YC, Lin PY, Yang J, Yang KH, Yang SC (2013) γ-Polyglutamic acid produced by Bacillus Subtilis (Natto): structural characteristics, chemical properties and biological functionalities. J Chin Chem Soc-Taip 53:1363–1384
Hu B, Wang J, Jin B, Li Y, Shi Z (2017) Assessment of the potential health risks of heavy metals in soils in a coastal industrial region of the Yangtze River Delta. Environ Sci Pollut R
Inbaraj BS, Chiu CP, Ho GH, Yang J, Chen BH (2008) Effects of temperature and pH on adsorption of basic brown 1 by the bacterial biopolymer poly(gamma-glutamic acid). Bioresour Technol 99:1026–1035
Inbaraj BS, Wang JS, Lu JF, Siao FY, Chen BH (2009) Adsorption of toxic mercury(II) by an extracellular biopolymer poly(γ-glutamic acid). Bioresour Technol 100:200–207
Iverson WP, Brinckman FE (1978) Microbial metabolism of heavy metals. Water pollution. Microbiology 2:201–232
Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207
Knight BP, Mcgrath SP, Chaudri AM (1997) Biomass carbon measurements and substrate utilization patterns of microbial populations from soils amended with cadmium, copper, or zinc. Appl Environ Microbiol 63:39–43
Koskan LP, Meah ARY, Sanders LJ, Ross RJ (1998) Method and composition for enhanced hydroponic plant productivity with polyamino acids. US
Lei P, Xu Z, Liang J, Luo X, Zhang Y, Feng X, Xu H (2016) Poly(γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus L. Plant Growth Regul 78:1–9
Lei P, Pang X, Feng X, Li S, Chi B, Wang R, Xu Z, Xu H (2017) The microbe-secreted isopeptide poly-γ-glutamic acid induces stress tolerance in Brassica napus L. seedlings by activating crosstalk between H2O2 and Ca2+. Sci Rep-UK 7:41618
Li Z, Xu J, Tang C, Wu J, Muhammad A, Wang H (2006) Application of 16S rDNA-PCR amplification and DGGE fingerprinting for detection of shift in microbial community diversity in Cu-, Zn-, and Cd-contaminated paddy soils. Chemosphere 62:1374–1380
Liao MT, Hedley MJ, Woolley DJ, Brooks RR, Nichols MA (2000) Copper uptake and translocation in chicory (Cichorium intybus L. cv. Grasslands Puna) and tomato (Lycopersicon esculentum Mill. cv. Rondy) plants grown in NFT system. I. Copper uptake and distribution in plants. Plant Soil 221:135–142
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382
Linger P, Ostwald A, Haensler J (2005) Cannabis sativa L. growing on heavy metal contaminated soil: growth, cadmium uptake and photosynthesis. Biol Plantarum 49:567–576
Liu X, Chi H, Yue M, Zhang X, Li W, Jia E (2012) The regulation of exogenous jasmonic acid on UV-B stress tolerance in wheat. J Plant Growth Regul 31:436–447
Meyer CL, Juraniec M, Huguet S, Chaves-Rodriguez E, Salis P, Isaure MP, Goormaghtigh E, Verbruggen N (2015) Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. J Exp Bot 66:3215–3227
Okamoto OK, Pinto E, Latorre LR, Bechara EJ, Colepicolo P (2001) Antioxidant modulation in response to metal-induced oxidative stress in algal chloroplasts. Arch Environ Con Tox 40:18–24
Page AL, Bingham FT, Nelson C (1972) Cadmium absorption and growth of various plant species as influenced by solution cadmium concentration. J Environ Qual 1:288–291
Pinto E, Sigaud Kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal induced oxidative stress in algae. J Phycol 39:1008–1018
Sonny SM, Crusberg TC, Dacunha CM, Iorio AAD (2006) A heavy metal biotrap for wastewater remediation using poly-γ-glutamic acid. Biotechnol Prog 22:523–531
Taiwo AM, Gbadebo AM, Oyedepo JA, Ojekunle ZO, Alo OM, Oyeniran AA, Onalaja OJ, Ogunjimi D, Taiwo OT (2015) Bioremediation of industrially contaminated soil using compost and plant technology. J Hazard Mater 304:166–172
Teh CY, Mahmood M, Shaharuddin NA, Chai LH (2015) In vitro rice shoot apices as simple model to study the effect of NaCl and the potential of exogenous proline and glutathione in mitigating salinity stress. Plant Growth Regul 75:1–11
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586
Wang TL, Kao TH, Inbaraj BS, Su YT, Chen BH (2010) Inhibition effect of poly(γ-glutamic acid) on lead-induced toxicity in mice. J Agr Food Chem 58:12562–12567
Wei M, Wu Y, Chen D, Gu Y (2010) Changes of free radicals and digestive enzymes in saliva in cases with deficiency in spleen-yin syndrome. J Biomed Res 24:250–255
Xiu L, Kunliang G, Hongxun Z (2012) Determination of microbial diversity in Daqu, a fermentation starter culture of Maotai liquor, using nested PCR-denaturing gradient gel electrophoresis. World J Microb Biot 28:2375–2381
Xu Z, Peng L, Feng X, Sha L, Hong X (2016) Analysis of the metabolic pathways affected by poly(γ-glutamic acid) in Arabidopsis thaliana based on genechip microarray. J Agr Food Chem 64:6257–6266
Yang ZH, Dong CD, Chen CW, Sheu YT, Kao CM (2017) Using poly-glutamic acid as soil-washing agent to remediate heavy metal-contaminated soils. Environ Sci Pollut R 1–12
Zhang Z (2015) Screening and assessment of solidification/stabilization amendments suitable for soils of lead-acid battery contaminated site. J Hazard Mater 288:140–146
Zhu J, Cai Z, Su X, Fu Q, Liu Y, Huang Q, Violante A, Hu H (2015) Immobilization and phytotoxicity of Pb in contaminated soil amended with γ-polyglutamic acid, phosphate rock, and γ-polyglutamic acid-activated phosphate rock. Environ Sci Pollut R 22:2661–2667
Funding
This work was funded by The Key Projects in the National Science & Technology Pillar Program during the Twelfth Five-year Plan Period (No. 2015BAD15B04), the National Nature Science Foundation of China (21506098), and the Natural Science Foundation of the Jiangsu (BK20150946).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Pang, X., Lei, P., Feng, X. et al. Poly-γ-glutamic acid, a bio-chelator, alleviates the toxicity of Cd and Pb in the soil and promotes the establishment of healthy Cucumis sativus L. seedling. Environ Sci Pollut Res 25, 19975–19988 (2018). https://doi.org/10.1007/s11356-018-1890-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-1890-9