Testing the ability of Vetiveria zizanioides plants to bind cadmium and its influence on soil microbial diversity

Abstract

Phytoremediation is an environmentally friendly and cost-effective approach for the remediation of heavy metals from contaminated environments. However, its effectiveness can be influenced by various factors, particularly the structure and diversity of soil microbial communities, which play a crucial role in enhancing or hindering the phytoremediation process. In this study, the remediation of cadmium-contaminated soil was investigated through the cultivation of Vetiveria zizanioides, examining its effects on the diversity of soil microbial communities. The concentration of Cd in roots and leaves reached more than 600 mg/kg DW and 400 mg/kg DW, respectively, at 60 mg/kg Cd treatment. Next-generation sequencing was used to characterize the soil microbial community. It was shown that the increased Cd contaminant from 20 mg/kg to 60 mg/kg of soil noticeably reduced the microbial count. A significant increase in species numbers was observed in the clean soil containing the V. zizanioides plants. In addition, soil samples from Cd-contaminated soil showed a considerable change in microbial structure at the genus level with the Sphingomonas bacteria becoming the most dominant genus against Cd-contamination.

Keywords

Phytoremediation / Cadmium remediation / Soil microbial composition / Soil contamination / Vetiveria zizanioides / Sphingomonas

Funding

The authors extend our gratitude to the personnel of the Research Institute of Petroleum Industry, Iran, for assisting us in this research project. (Project No. 33481249).

Conflict of interest

The authors declare that there is no conflict of interest.

References

[1] Bhavya P, Madasseri S, Gowthamchand NJ, Anil S. Soil contamination and remediation. In: Modern Approaches in Soil Science. 2^nd ed., Vol. 2. Haryana:Stella International Publication; 2024.

[2] Debonne N, Van Vliet J, Metternicht G, Verburg P. Agency shifts in agricultural land governance and their implications for land degradation neutrality. Glob Environ Change. 2021; 66:102221. doi: 10.1016/j.gloenvcha.2020.102221

[3] Bernardino CA, Mahler CF, Alvarenga P, et al. Recent advances in phytoremediation of soil contaminated by industrial waste:A roadmap to a safer environment. In: Bioremediation of Industrial Waste and Environmental Safety. Germany: Springer; 2019. p. 207-21.

[4] Zhang Z, Wang X, Jiang H. Sunflower (Helianthus annuus) and its role in Cd uptake and remediation. Environ Sci Pollut Res Int. 2019; 26(3):3055-3064. doi: 10.1007/s11356-018-3801-9

[5] Shaw DR, Dussan J. Mathematical modeling of toxic metal uptake and efflux pump in metal-resistant bacterium Bacillus cereus isolated from heavy crude oil. Water Air Soil Pollut. 2015; 226(4):2385. doi: 10.1007/s11270-015-2385-7

[6] Gondal MA, Aldakheel RK, Almessiere MA, et al. Determination of heavy metals in cancerous and healthy colon tissues using laser-induced breakdown spectroscopy and cross-validation with ICP-AES method. J Pharm Biomed Anal. 2020; 183:113153. doi: 10.1016/j.jpba.2020.113153

[7] Abdel-Shafy IH, Mansour SM. environmental impact, A review on polycyclic aromatic hydrocarbons: Source, effect on human health and remediation. Egypt J Pet. 2016; 25:107-123. doi: 10.1016/j.ejpe.2015.03.011

[8] Han X, Tianyi C, Sun T. Study on Heavy Metal Pollution Characteristics and Its Health Risk Assessment From Sludge of Sewage Treatment Plants in Industrial Parks [Preprint]; 2020. doi: 10.21203/rs.3.rs-34745/v1

[9] Yang X, Liu L, Tan W, Liu C, Dang Z, Qiu G. Remediation of heavy metal contaminated soils by organic acid extraction and electrochemical adsorption. Environ Pollut. 2020; 264:114745. doi: 10.1016/j.envpol.2020.114745

[10] Abdin Y, Adel U, Yong SK, Yiu Fai T, Al-Wabel M. Competitive sorption and availability of coexisting heavy metals in mining-contaminated soil: Contrasting effects of mesquite and fishbone biochars. Environ Res. 2020; 181:108846. doi: 10.1016/j.envres.2019.108846

[11] Akhtar FZ, Archana KM, Krishnaswamy VG, Rajagopal R. Remediation of heavy metals (Cr, Zn) using physical, chemical and biological methods: A novel approach. SN Appl Sci. 2020; 2:1918. doi: 10.1007/s42452-019-1918-x

[12] Haq S, Bhatti AA, Dar ZA, Bhat SA.Phytoremediation of heavy metals: An eco-friendly and sustainable approach. In: Hakeem KR, Bhat SA, Qadri H, editors. Bioremediation and Biotechnology, Sustainable Approaches to Pollution Degradation. Germany: Springer; 2020. p. 215-231. doi: 10.1007/978-3-030-35691-0_10

[13] Muthusaravanan S, Sivarajasekar N, Vivek JS.Research updates on heavy metal phytoremediation: Enhancements, efficient post-harvesting strategies and economic opportunities. In: Inamuddin, Ahamed MI, Lichtfouse E, editors. Environmental Chemistry for a Sustainable World. Germany: Springer; 2020. p. 191-222. doi: 10.1007/978-3-030-17724-9_9

[14] Farraji H, Robinson B, Mohajeri P, Abedi T. Phytoremediation: Green technology for improving aquatic and terrestrial environments. Nippon J Environ Sci. 2021; 1:1002. doi: 10.46266/njes.1002

[15] Wani KA, Sofi ZM, Malik JA, Wani JA. Phytoremediation of heavy metals using Salix (willows). In: Hakeem KR, Bhat SA, Qadri H, editors. Bioremediation and Biotechnology. Cham: Springer; 2020. p. 161-174. doi: 10.1007/978-3-030-40333-1_9

[16] Manoj SR, Karthik C, Kadirvelu K. Understanding the molecular mechanisms for the enhanced phytoremediation of heavy metals through plant growth-promoting rhizobacteria: A review. J Environ Manage. 2020; 254:109779. doi: 10.1016/j.jenvman.2019.109779

[17] Awa SH, Hadibarata T. Removal of heavy metals in contaminated soil by phytoremediation mechanism: A review. Water Air Soil Pollut. 2020; 231(2):47.

[18] Almeida A, Ribeiro C, Carvalho F, et al. Phytoremediation potential of Vetiveria zizanioides and Oryza sativa for nitrate and organic substance removal in vertical flow constructed wetlands. Ecol Eng. 2019; 138:19-27. doi: 10.1016/j.ecoleng.2019.06.020

[19] Chen HM, Zheng CR, Tu C, Shen ZG. Chemical methods and phytoremediation of soil contaminated with heavy metals. Chemosphere. 2000; 41:229-234. doi: 10.1016/s0045-6535(99)00415-4

[20] Bhati T, Gupta R, Yadav N, et al. Assessment of bioremediation potential of Cellulosimicrobium sp. for treatment of multiple heavy metals. Microbiol Biotechnol Lett. 2019; 47:269-277. doi: 10.4014/mbl.1808.08006

[21] Tang H, Xiang G, Xiao W, Yang Z, Zhao B. Microbial mediated remediation of heavy metals toxicity: Mechanisms and future prospects. Front Plant Sci. 2024; 15:1420408. doi: 10.3389/fpls.2024.1420408

[22] Abdallah RS, Arief R, Yanuwiadi B. Phytoremediation of lead-contaminated soil using vetiver grass (Vetiveria zizanioides L.). J Exp Life Sci. 2019; 9:54-59. doi: 10.21776/ub.jels.2019.009.01.09

[23] Kiamarsi Z, Kafi M, Soleimani M, Nezami A, Lutts S. Conjunction of Vetiveria zizanioides L. and oil-degrading bacteria as a promising technique for remediation of crude oil-contaminated soils. J Clean Prod. 2020; 253:119719. doi: 10.1016/j.jclepro.2019.119719

[24] Liu H, Xie Y, Li J, et al. Effect of Serratia sp. K3 combined with organic materials on cadmium migration in soil- Vetiveria zizanioides L. system and bacterial community in contaminated soil. Chemosphere. 2020; 242:125164. doi: 10.1016/j.chemosphere.2019.125164

[25] Thijs S, Sillen W, Weyens N, Vangronsveld J. Phytoremediation: State-of-the-art and a key role for the plant microbiome in future trends and research prospects. Int J Phytoremediation. 2016; 19(1):23-38. doi: 10.1080/15226514.2016.1216076

[26] Ng YS, Shen ZG, Li XD. Modification of heavy metal phytoremediation using Vetiveria zizanioides by EDTA addition into soil. Environ Pollut. 2004; 128(1-2):73-84. doi: 10.1016/j.envpol.2003.08.011

[27] Martínez-Espinosa RM. Microorganisms and their metabolic capabilities in the context of the biogeochemical nitrogen cycle at extreme environments. Int J Mol Sci. 2020; 21(12):4228. doi: 10.3390/ijms21124228

[28] Effendi H, Bagus W, Utomo A, Pratiwi NT. Ammonia and orthophosphate removal of tilapia cultivation wastewater with Vetiveria zizanioides. J King Saud Univ Sci. 2018; 32:207-212. doi: 10.1016/j.jksus.2018.04.018

[29] Shah V, Daverey A. Phytoremediation: A multidisciplinary approach to clean up heavy metal-contaminated soil. Environ Technol Innov. 2020; 18:100774. doi: 10.1016/j.eti.2020.100774

[30] Borralho T, Gago D, Almeida A. Application of floating beds of macrophytes (Vetiveria zizanioides and Phragmites australis) for heavy metal removal in Água Forte Stream (Alentejo-Portugal). J Ecol Eng. 2020; 21:153-163. doi: 10.12911/22998993/118285

[31] Long Y, Yi H, Chen S, et al. Influences of plant type on bacterial and archaeal communities in constructed wetlands treating polluted river water. Environ Sci Pollut Res Int. 2016; 23(19):19570-19579. doi: 10.1007/s11356-016-7166-3

[32] Pan J, Yu L. Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecol Eng. 2011; 37(11):1889-1894. doi: 10.1016/j.ecoleng.2011.07.002

[33] Salman S, Salman A, Zeid SA, Seleem EM, Abdel- Hafiz MA. Soil characterization and heavy metal pollution assessment in Orabi farms, El Obour, Egypt. Bull Natl Res Cent. 2019; 43(1):82. doi: 10.1186/s42269-019-0082-1

[34] Parvin T, Salilih MF, Ishetu AI. Microbes used as a tool for bioremediation of heavy metal from the environment. Cogent Food Agric. 2020; 6(1):1783174. doi: 10.1080/23311932.2020.1783174

[35] Liu Y, Nuza’aiti A, Zeng G, et al. Cadmium accumulation in Vetiveria zizanioides and its effects on growth, physiological and biochemical characters. Bioresour Technol. 2010; 101(17):6297-6303. doi: 10.1016/j.biortech.2010.03.02

[36] Rana MS, Meena VS, Kour A. Brassica juncea for Cd removal: A comparative study. J Environ Manage. 2021; 289:112537. doi: 10.1016/j.jenvman.2021.112537

[37] Aibibu N, Liu Y, Zeng G, et al. Cadmium accumulation in Vetiveria zizanioides and its effects on growth, physiological and biochemical characters. Bioresour Technol. 2010; 101:6297-6303. doi: 10.1016/j.biortech.2010.03.028

[38] Gohari S, Ghaffari H, Asadi A. Mechanisms of heavy metal tolerance in Cicer arietinum under Cd stress. Environ Toxicol Chem. 2020; 39(1):124-133.

[39] Yu SH, Deng HP, Zhang B, et al. Physiological response of Vetiveria zizanioides to cadmium stress revealed by Fourier transform infrared spectroscopy. Spectrochim Acta A Mol Biomol Spectrosc. 2017; 55(3):157-165. doi: 10.1080/00387010.2017.1355321

[40] Zheng S, Wang Q, Yuan Y, Sun W. Human health risk assessment of heavy metals in soil and food crops in the Pearl River Delta urban agglomeration of China. Food Chem. 2020; 316:126213. doi: 10.1016/j.foodchem.2020.126213

[41] Phusantisampan T, Meeinkuirt W, Saengwilai P, Pichtel J, Chaiyarat R. Phytostabilization potential of two ecotypes of Vetiveria zizanioides in cadmium-contaminated soils: Greenhouse and field experiments. Environ Sci Pollut Res Int. 2016; 23(20):20027-20038. doi: 10.1007/s11356-016-7229-5

[42] Anglana C, Capaci P, Barozzi F, et al. Dittrichia viscosa selection strategy based on stress produces stable clonal lines for phytoremediation applications. Plants (Basel). 2023; 12(13):2499. doi: 10.3390/plants12132499

[43] Calcagnile M, Tredici SM, Talà A, Alifano P. Bacterial semiochemicals and transkingdom interactions with insects and plants. Insects. 2019; 10(12):441. doi: 10.3390/insects10120441

[44] Lorenz N, Hintemann T, Kramarewa T. Response of microbial activity and microbial community composition in soils to long-term arsenic and cadmium exposure. Soil Biol Biochem. 2006; 38(6):1430-1437. doi: 10.1016/j.soilbio.2005.10.020

[45] Wang L, Liu S, Li J, Li S. Effects of several organic fertilizers on heavy metal passivation in Cd-contaminated gray-purple soil. Front Environ Sci. 2022; 10:895646. doi: 10.3389/fenvs.2022.895646

[46] Zhou Q, Zhang J, Wang X, Li F. Field applications of phytoremediation for heavy metal-contaminated soils. Environ Sci Pollut Res Int. 2020; 27(4):3721-3732. doi: 10.1007/s11356-019-07243-3

[47] Singh P, Prasad SM. Phytoremediation of heavy metals: Concepts, methods, and applications. Environ Monit Assess. 2019; 191(1):30. doi: 10.1007/s10661-018-7159-x

[48] Ali H, Khan E, Sajad MA. Phytoremediation of heavy metals-concepts and applications. Chem Eng J. 2013; 226:396-404. doi: 10.1016/j.chemosphere.2013.01.075

[49] Pischke E, Barozzi F, Colina Blanco AE, et al. Dimethylmonothioarsenate is highly toxic for plants and readily translocated to shoots. Environ Sci Technol. 2022; 56(14):10072-10083. doi: 10.1021/acs.est.2c01206

[50] United States Environmental Protection Agency. (1999). Phytoremediation Resource Guide (EPA 542-B-99-003). Office of Solid Waste and Emergency Response.

[51] Mahajan P, Kaushal J. Role of phytoremediation in reducing cadmium toxicity in soil and water. J Toxicol. 2018; 2018:4864365. doi: 10.1155/2018/4864365