Abstract
In this investigation the heavy metals (Cu, Zn, Mn, Cr and Ni) remediation potential of Eisenia fetida was studied in the crude oil polluted soil. The potential of E. fetida was evaluated based on the decrease in concentrations of Cu, Zn, Mn, Cr and Ni, and improvement in the soil enzyme activities at the end of 90 days of experimental trials. Moreover, soil health quality, inter-relationship between the enzyme activities and the growth parameters of E. fetida and synergistic relation among the enzyme activities were also evaluated through G-Mean and T-QSI indices, chord plot analysis and principal component analysis (PCA) to confirm the performance of E. fetida during vermiremediation. The results revealed that the soil treated with E. fetida showed a reduction in the concentration of Cu, Zn, Mn, Cr and Ni by 17.4% 19.45%, 9.44%, 23.8% and 9.6% respectively by end of the experimental trials. The cellulase, amylase, polyphenol oxidase, peroxidase, urease, dehydrogenase and catalase activities in the E. fetida-treated soil were enhanced by 89.83%, 99.17%, 142%, 109.9%, 92.9%, 694.3% and 274.5% respectively. The results of SEM-EDS revealed enhancement in the O, K, Na, Mg and P content by 62.36%, 96.2%, 97.9%, 93.7% and 98.2% respectively by the end of the experimental trial. The G-Mean and T-QSI indices also confirmed the improvement in soil enzyme activities thereby indicating the positive influence of E. fetida on soil decontamination process. The chord plot indicated the interrelationship between the earthworm’s growth parameters and enzyme activities of the soil as indicated by the high linkage between the nodes. Finally, the PCA confirmed the negative effect of the heavy metals on the soil enzyme activities and synergistic interrelationship between the enzyme activities during the vermiremediation process. Thus, this study demonstrated the changes in the soil enzyme activities and their interconnected influences during vermiremediation of crude oil sourced heavy metals from polluted soil.
Similar content being viewed by others
Data availability
The data reported in the current study have been obtained in original upon experimentation. The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.
References
Adetunji AT, Lewu FB, Mulidzi R, Ncube B (2017) The biological activities of β-glucosidase, phosphatase and urease as soil quality indicators: a review. J Soil Sci Plant Nutr 17(3):794–807. https://doi.org/10.4067/S0718-95162017000300018
Al-Moaikal RMS, Shukry WM, Azzoz MM, Al-Hawas GHS (2012) Effect of crude oil on germination, growth and seed protein profile of Jojoba (Simmodsiachinensis). Plant Sci J 1:20–35. https://doi.org/10.13140/2.1.3537.4087
Ameen F, Al-Homaidan AA (2022) Treatment of heavy metal–polluted sewage sludge using biochar amendments and vermistabilization. Environ Monit Assess 194(12):861. https://doi.org/10.1007/s10661-022-10559-x
Aponte H, Meli P, Butler B, Paolini J, Matus F, Merino C et al (2020) Meta-analysis of heavy metal effects on soil enzyme activities. Sci Total Environ 737:139744. https://doi.org/10.1016/j.scitotenv.2020.139744
Baruah N, Mondal SC, Farooq M, Gogoi N (2019) Influence of heavy metals on seed germination and seedling growth of wheat, pea, and tomato. Water Air Soil Pollut 230(12):1–15. https://doi.org/10.1007/s11270-019-4329-0
Borah G, Deka H (2023) Crude oil associated heavy metals (HMs) contamination in agricultural land: understanding risk factors and changes in soil biological properties. Chemosphere 310:136890. https://doi.org/10.1016/j.chemosphere.2022.136890
Boruah T, Barman A, Kalita P, Lahkar J, Deka H (2019) Vermicomposting of citronella bagasse and paper mill sludge mixture employing Eisenia fetida. Bioresour Technol 294:122147. https://doi.org/10.1016/j.biortech.2019.122147
Cao J, Wang C, Ji D (2016) Improvement of the soil nitrogen content and maize growth by earthworms and arbuscular mycorrhizal fungi in soils polluted by oxytetracycline. Sci Total Environ 571:926–934. https://doi.org/10.1016/j.scitotenv.2016.07.077
Cao X, Bi R, Song Y (2017) Toxic responses of cytochrome P450 sub-enzyme activities to heavy metals exposure in soil and correlation with their bioaccumulation in Eisenia fetida. Ecotoxicol Environ Saf 144:158–165. https://doi.org/10.1016/j.ecoenv.2017.06.023
Cao X, Cai C, Wang Y, Zheng X (2018) The inactivation kinetics of polyphenol oxidase and peroxidase in bayberry juice during thermal and ultrasound treatments. Innovative Food Sci Emerg Technol 45:169–178. https://doi.org/10.1016/j.ifset.2017.09.018
Cao X, Ma R, Zhang Q, Wang W, Liao Q, Sun S et al (2020) The factors influencing sludge incineration residue (SIR)-based magnesium potassium phosphate cement and the solidification/stabilization characteristics and mechanisms of heavy metals. Chemosphere 261:127789. https://doi.org/10.1016/j.chemosphere.2020.127789
Chachina SB, Voronkova NA, Baklanova ON (2015) Biological remediation of the engine lubricant oil-contaminated soil with three kinds of earthworms, Eisenia fetida, Eisenia andrei, Dendrobenaveneta, and a mixture of microorganisms. Procedia Eng 113:113–123. https://doi.org/10.1016/j.proeng.2015.07.302
Cheng Q, Lu C, Shen H, Yang Y, Chen H (2021) The dual beneficial effects of vermiremediation: reducing soil bioavailability of cadmium (Cd) and improving soil fertility by earthworm (Eisenia fetida) modified by seasonality. Sci Total Environ 755:142631. https://doi.org/10.1016/j.scitotenv.2020.142631
Cleophas FN, Zahari NZ, Murugayah P, Rahim SA, Mohd Yatim AN (2022) Phytoremediation: a novel approach of bast fiber plants (hemp, kenaf, jute and flax) for heavy metals decontamination in soil. Toxics 11(1):5. https://doi.org/10.3390/toxics11010005
Cui J, Cui J, Li J, Wang W, Xu B, Yang J et al (2023) Improving earthworm quality and complex metal removal from water by adding aquatic plant residues to cattle manure. J Hazard Mater 443:130145. https://doi.org/10.1016/j.jhazmat.2022.130145
Ekperusi OA, Aigbodion IF, Iloba BN, Okorefe S (2016) Assessment and bioremediation of heavy metals from crude oil contaminated soil by earthworms. Ethiop J Environ Stud Manag 9(2):1036-1046.ISSN:1998-0507. https://doi.org/10.4314/ejesm.v9i2.9S
Feria-Cáceres PF, Penagos-Velez L, Moreno-Herrera CX (2022) Tolerance and cadmium (Cd) immobilization by native bacteria isolated in cocoa soils with increased metal content. Microbiol Res 13(3):556–573. https://doi.org/10.3390/microbiolres13030039
Ghazal H, Koumaki E, Hoslett J, Malamis S, Katsou E, Barcelo D, Jouhara H (2022) Insights into current physical, chemical and hybrid technologies used for the treatment of wastewater contaminated with pharmaceuticals. J Clean Prod 361:132079. https://doi.org/10.1016/j.jclepro.2022.132079
Gusain R, Suthar S (2020) Vermicomposting of duckweed (Spirodelapolyrhiza) by employing Eisenia fetida: changes in nutrient contents, microbial enzyme activities and earthworm biodynamics. Bioresour Technol 311:123585. https://doi.org/10.1016/j.biortech.2020.123585
Hussain Qaiser MS, Ahmad I, Ahmad SR, Afzal M, Qayyum A (2019) Assessing heavy metal contamination in oil and gas well drilling waste and soil in Pakistan. Pol J Environ Stud 28(2). https://doi.org/10.15244/pjoes/85301
Jahirul MI, Rasul MG, Brown RJ, Senadeera W, Hosen MA, Haque R, Saha SC, Mahlia TMI (2021) Investigation of correlation between chemical composition and properties of biodiesel using principal component analysis (PCA) and artificial neural network (ANN). Renew Energy 168(632–646):483. https://doi.org/10.1016/j.renene.2020.12.078
Johnson JI, Temple KL (1964) Some variables affecting the measurement of catalase activity in soil. Soil Sci Soc Am Proc 28:207–216. https://doi.org/10.2136/sssaj1964.03615995002800020024x
Koolivand A, Saeedi R, Coulon F, Kumar V, Villaseñor J, Asghari F, Hesampoor F (2020) Bioremediation of petroleum hydrocarbons by vermicomposting process bioaugmentated with indigenous bacterial consortium isolated from petroleum oily sludge. Ecotoxicol Environ Saf 198:110645
Kotoky P, Bora BJ, Baruah NK, Baruah J, Baruah P, Borah GC (2003) Chemical fractionation of heavy metals in soils around oil installations, Assam. Chem Speciat Bioavailab 15(4):115–126. https://doi.org/10.3184/095422903782775181
Lai W, Wu Y, Zhang C, Dilinuer Y, Pasang L, Lu Y et al (2022) Combination of biochar and phosphorus solubilizing bacteria to improve the stable form of toxic metal minerals and microbial abundance in Lead/Cadmium-contaminated soil. Agronomy 12(5):1003. https://doi.org/10.3390/agronomy12051003
Lemtiri A, Liénard A, Alabi T, Brostaux Y, Cluzeau D, Francis F, Colinet G (2016) Earthworms Eisenia fetida affect the uptake of heavy metals by plants Vicia faba and Zea mays in metal-contaminated soils. Appl Soil Ecol 104:67–78. https://doi.org/10.1016/j.apsoil.2015.11.021
Mallampati SR, Mitoma Y, Okuda T, Sakita S, Kakeda M (2013) Total immobilization of soil heavy metals with nano-Fe/Ca/CaO dispersion mixtures. Environ Chem Lett 11:119–125. https://doi.org/10.1007/s10311-012-0384-0
Medina-Sauza RM, Álvarez-Jiménez M, Delhal A, Reverchon F, Blouin M, Guerrero-Analco JA et al (2019) Earthworms building up soil microbiota, a review. Front Environ Sci 7:81. https://doi.org/10.3389/fenvs.2019.00081
Munir MAM, Yousaf B, Ali MU, Dan C, Abbas Q, Arif M, Yang X (2021) In situ synthesis of micro-plastics embedded sewage-sludge co-pyrolyzed biochar: implications for the remediation of Cr and Pb availability and enzymatic activities from the contaminated soil. J Clean Prod 302:127005. https://doi.org/10.1016/j.jclepro.2021.127005
Ordoñez-Arévalo B, Guillén-Navarro K, Huerta E, Cuevas R, Calixto-Romo MA (2018) Enzymatic dynamics into the Eisenia fetida (Savigny, 1826) gut during vermicomposting of coffee husk and market waste in a tropical environment. Environ Sci Pollut Res 25:1576–1586
Pancholy SK, Rice EL, Turner JA (1975) Soil factors preventing revegetation of a denuded area near an abandoned zinc smelter in Oklahoma. J Appl Ecol 12(1):337–342 https://www.jstor.org/stable/2401736
Parelho C, Rodrigues A, do Carmo Barreto M, Cruz JV, Rasche F, Silva L, Garcia P (2021) Bioaccumulation and potential ecotoxicological effects of trace metals along a management intensity gradient in volcanic pasturelands. Chemosphere 273:128601. https://doi.org/10.1016/j.chemosphere.2020.128601
Patel AB, Shaikh S, Jain KR, Desai C, Madamwar D (2020) Polycyclic aromatic hydrocarbons: sources, toxicity, and remediation approaches. Front Microbiol 11:562813. https://doi.org/10.3389/fmicb.2020.562813
Paul S, Das S, Raul P, Bhattacharya SS (2018) Vermi-sanitization of toxic silk industry waste employing Eisenia fetida and Eudrilus eugeniae: substrate compatibility, nutrient enrichment and metal accumulation dynamics. Bioresour Technol 266:267–274. https://doi.org/10.1016/j.biortech.2018.06.092
Paz-Ferreiro J, Fu S (2016) Biological indices for soil quality evaluation: perspectives and limitations. Land Degrad Dev 27(1):14–25. https://doi.org/10.1002/ldr.2262
Rajadurai M, Karmegam N, Kannan S, Yuvaraj A, Thangaraj R (2022) Vermiremediation of engine oil contaminated soil employing indigenous earthworms, Drawidamodesta and Lampitomauritii. J Environ Manag 301:113849. https://doi.org/10.1016/j.jenvman.2021.113849
Rashmi I, Roy T, Kartika KS, Pal R, Coumar V, Kala S, Shinoji KC (2020) Organic and inorganic fertilizer contaminants in agriculture: impact on soil and water resources. Contaminants in Agriculture:3–41. https://doi.org/10.1007/978-3-030-41552-5_1
Rich N, Bharti A, Kumar S (2018) Effect of bulking agents and cow dung as inoculant on vegetable waste compost quality. Bioresour Technol 252:83–90. https://doi.org/10.1016/j.biortech.2017.12.080
Roberge MR (1978) Methodology of enzymes determination and extraction. In: Burns RG (ed) Soil enzymes. Academic Press, New York, pp 341–373. https://doi.org/10.1016/B978-012513840-6/50022-7
Sanchez-Hernandez JC, Del Pino JN, Capowiez Y, Mazzia C, Rault M (2018) Soil enzyme dynamics in chlorpyrifos-treated soils under the influence of earthworms. Sci Total Environ 612:1407–1416. https://doi.org/10.1016/j.scitotenv.2017.09.043
Shameema KP, Chinnamma MA (2018) Vermiremediation of heavy metal contaminated soil. Int J Adv Inf Eng Technol 5(4):32–38
Singh BM, Singh D, Dhal NK (2022) Enhanced phytoremediation strategy for sustainable management of heavy metals and radionuclides. Case Stud Chem Environ Eng 5:100176. https://doi.org/10.1016/j.cscee.2021.100176
Sohal B, Bhat SA, Vig AP (2021) Vermiremediation and comparative exploration of physicochemical, growth parameters, nutrients and heavy metals content of biomedical waste ash via ecosystem engineers Eisenia fetida. Ecotoxicol Environ Saf 227:112891. https://doi.org/10.1016/j.ecoenv.2021.112891
Sun W, Zhu B, Yang F, Dai M, Sehar S, Peng C et al (2021) Optimization of biosurfactant production from Pseudomonas sp. CQ2 and its application for remediation of heavy metal contaminated soil. Chemosphere 265:129090. https://doi.org/10.1016/j.chemosphere.2020.129090
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1(4):301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Tang J, Zhang L, Zhang J, Ren L, Zhou Y, Zheng Y et al (2020) Physicochemical features, metal availability and enzyme activity in heavy metal-polluted soil remediated by biochar and compost. Sci Total Environ 701:134751. https://doi.org/10.1016/j.scitotenv.2019.134751
Ukalska-Jaruga A, Siebielec G, Siebielec S, Pecio M (2022) The effect of soil amendments on trace elements’ bioavailability and toxicity to earthworms in contaminated soils. Appl Sci 12(12):6280. https://doi.org/10.3390/app12126280
Van Elsas JD, Pratama AA, de Araujo WL, Trevors JT (2019) Microbial interactions in soil. In: Modern soil microbiology, third edition. CRC Press, pp 141–161
Wang G, Pan X, Zhang S, Zhong Q, Zhou W, Zhang X et al (2020) Remediation of heavy metal contaminated soil by biodegradable chelator–induced washing: efficiencies and mechanisms. Environ Res 186:109554. https://doi.org/10.1016/j.envres.2020.109554
Wang G, Wang L, Ma F, Yang D, You Y (2021) Earthworm and arbuscular mycorrhiza interactions: strategies to motivate antioxidant responses and improve soil functionality. Environ Pollut 272:115980. https://doi.org/10.1016/j.envpol.2020.115980
Wang Q, Ma M, Jiang X, Guan D, Wei D, Zhao B et al (2019a) Impact of 36 years of nitrogen fertilization on microbial community composition and soil carbon cycling-related enzyme activities in rhizospheres and bulk soils in northeast China. Appl Soil Ecol 136:148–157. https://doi.org/10.1016/j.apsoil.2018.12.019
Wang Y, Wang HS, Tang CS, Gu K, Shi B (2019b) Remediation of heavy-metal-contaminated soils by biochar: a review. Environ Geotech 9(3):135–148. https://doi.org/10.1680/jenge.18.00091
Warman PR (1999) Evaluation of seed germination and growth tests for assessing compost maturity. Compost Sci Util 7(3):33–37. https://doi.org/10.1080/1065657X.1999.10701972
Xiao R, Ali A, Xu Y, Abdelrahman H, Li R, Lin Y et al (2022) Earthworms as candidates for remediation of potentially toxic elements contaminated soils and mitigating the environmental and human health risks: a review. Environ Int 158:106924. https://doi.org/10.1016/j.envint.2021.106924
Xu K, Liu YX, Wang XF, Li SW, Cheng JM (2020) Combined toxicity of functionalized nano-carbon black and cadmium on Eisenia fetida coelomocytes: the role of adsorption. J Hazard Mater 398:122815. https://doi.org/10.1016/j.jhazmat.2020.122815
Xu Z, Yang Z, Zhu T, Shu W, Geng L (2021) Ecological improvement of antimony and cadmium contaminated soil by earthworm Eisenia fetida: Soil enzyme and microorganism diversity. Chemosphere 273:129496. https://doi.org/10.1016/j.chemosphere.2020.129496
Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z (2020) Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:359. https://doi.org/10.3389/fpls.2020.00359
Yano K, Morinaka Y, Wang F, Huang P, Takehara S, Hirai T, Ito A, Koketsu E, Kawamura M, Kotake K, Yoshida S, Endo M, Tamiya G, Kitano H, Ueguchi-Tanaka M, Hirano K, Matsuoka M (2019) GWAS with principal component analysis identifies a gene comprehensively controlling rice architecture. Proc Natl Acad Sci 116:2162–21267. https://doi.org/10.1073/pnas.1904964116
Yuvaraj A, Govarthanan M, Karmegam N, Biruntha M, Kumar DS, Arthanari M et al (2021) Metallothionein dependent-detoxification of heavy metals in the agricultural field soil of industrial area: earthworm as field experimental model system. Chemosphere 267:129240. https://doi.org/10.1016/j.chemosphere.2020.129240
Zeng XY, Li SW, Leng Y, Kang XH (2020) Structural and functional responses of bacterial and fungal communities to multiple heavy metal exposure in arid loess. Sci Total Environ 723:138081. https://doi.org/10.1016/j.scitotenv.2020.138081
Zhang D, Yin C, Abbas N, Mao Z, Zhang Y (2020) Multiple heavy metal tolerance and removal by an earthworm gut fungus Trichodermabrevicompactum QYCD-6. Sci Rep 10(1):1–9. https://doi.org/10.1038/s41598-020-63813-y
Zhou Y, Li H, Guo W, Liu H, Cai M (2022) The synergistic effect between biofertility properties and biological activities in vermicomposting: a comparable study of pig manure. J Environ Manag 324:116280. https://doi.org/10.1016/j.jenvman.2022.116280
Acknowledgements
The authors are thankful to the Department of Botany, Gauhati University, Assam, India, for providing the basic laboratory facilities to carry out the work smoothly.
Code availability
Not applicable
Author information
Authors and Affiliations
Contributions
HD provided laboratory facilities and guided GB for PhD. GB carried out the experimental works, analysis and statistical work, and wrote the MS under direct supervision of HD.
Corresponding author
Ethics declarations
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Chris Lowe
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 57 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Borah, G., Deka, H. Vermiremediation of heavy metals (HMs)-contaminated agricultural land: synergistic changes in soil enzyme activities and earthworm’s growth parameters. Environ Sci Pollut Res 30, 115266–115278 (2023). https://doi.org/10.1007/s11356-023-30500-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-30500-0