Skip to main content

Advertisement

Log in

Rhizoremediation of Cd-contaminated soil using Zea mays Sturt, with heavy metal resistant rhizobacteria that alleviate Cd-induced stress in plant

  • Original Article
  • Published:
Environmental Sustainability Aims and scope Submit manuscript

Abstract

Exposure to a high concentration of cadmium (Cd) is toxic to living organisms. The present study deals with the characterization of Cd resistant bacterial isolates, and analysis of the rhizoremediation of Cd using the metal resistant plant growth promoting (PGP) rhizobacteria applied through maize (Zea mays Sturt) rhizosphere. Cd resistant bacterial isolates were selected, analyzed for PGP attributes and applied in the rhizosphere of maize plants to study their effects on plant growth under metal stress, along with the Cd rhizoremediation potential. The bacterial isolates Serratia marcescens S2I7, S. marcescens BB-2B, Bacillus subtilis SR1 and Paenibacillus sp. S1I8 showed resistance to Cd and positive for PGP attributes, like phosphate-solubilization, production of indole acetic acid (IAA), and siderophore. The augmentation of the metal resistant bacteria caused 26% increase in the shoot length of the plants in Cd spiked soil. Under the stress of Cd, the activity of stress-responsive enzymes- glutathione S-transferase (GST), catalase (CAT), peroxidases (POD) of the treated plants were relatively higher. Augmentation of the bacterial isolates significantly reduced the activity of stress-responsive enzymes. The association of Z. mays-rhizobacteria played the most crucial role in the process of bioremediation, as it could remove up to 31% of Cd from soil after 30 days. The present study emphasizes the efficiency of plant–microbe interactions in the rhizosphere to remove metals from soil through the promotion of plant growth in contaminated sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The 16 s rDNA sequences of the isolates have been submitted to the National Centre for Biotechnology Information (NCBI) genebank database under the accession numbers MF992191 (B. subtilis SR1), KX602663 (Paenibacillus sp. S1I8), MF554655 (S. marcescens BB-2B), and KY744360 (S. marcescens S2I7).

References

  • Aladesanmi OT, Oroboade JG, Osisiogu CP, Osewole AO (2019) Bioaccumulation factor of selected heavy metals in Zea mays. J Health Pollut 9:24

    Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—Concepts and applications. Chemosphere 91:869–881

    Article  CAS  Google Scholar 

  • Bashir S, Hussain Q, Akmal M, Riaz M, Hu H, Ijaz SS, Iqbal M, Abro S, Mehmood S, Ahmad M (2018a) Sugarcane bagasse-derived biochar reduces the cadmium and chromium bioavailability to mash bean and enhances the microbial activity in contaminated soil. J Soils Sedim 18:874–886

    Article  CAS  Google Scholar 

  • Bashir S, Hussain Q, Shaaban M, Hu H (2018b) Efficiency and surface characterization of different plant-derived biochar for cadmium (Cd) mobility, bioaccessibility and bioavailability to Chinese cabbage in highly contaminated soil. Chemosphere 211:632–639

    Article  CAS  Google Scholar 

  • Becerra-Castro C, Prieto-Fernandez A, Alvarez-Lopez V, Monterroso C, Cabello-Conejo MI, Acea MJ, Kidd PS (2011) Nickel solubilizing capacity and characterization of rhizobacteria isolated from hyperaccumulating and non-hyperaccumulating subspecies of Alyssum serpyllifolium. Int J Phytoremediat 1:229–244

    Article  Google Scholar 

  • Belyaeva ON, Haynes RJ, Birukova OA (2005) Barley yield and soil microbial and enzyme activities as affected by contamination of two soils with lead, zinc or copper. Biol Fertil Soils 41(2):85–94

    Article  CAS  Google Scholar 

  • Bojorquez C, Voltolina D (2016) Removal of cadmium and lead by adapted strains of Pseudomonas aeruginosa and Enterobacter cloacae. Rev Int Contam Ambie 32:407–412

    Article  CAS  Google Scholar 

  • Brunetti G, Farrag K, Rovira PS, Nigro F, Senesi N (2011) Greenhouse and field studies on Cr, Cu, Pb and Zn phytoextraction by Brassica napus from contaminated soils in the Apulia region, Southern Italy. Geoderma 160(3–4):517–523

    Article  CAS  Google Scholar 

  • Caregnato FF, Koller CE, MacFarlane GR, Moreira JCF (2008) The glutathione antioxidant system as a biomarker suite for the assessment of heavy metal exposure and effect in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull 56:1119–1127

    Article  CAS  Google Scholar 

  • Chibuike GU, Obiora SC (2014) Heavy metal polluted soils: effect on plants and bioremediation methods. Appl Environ Soil Sci 2:12

    Google Scholar 

  • Dey S, Mazumder PB, Paul SB (2014) Accumulation of Cu at different concentration in tea plant (Camellia sinensis(L) OKuntze). IOSR J Agric Vet Sci 7(4):39–43

    Article  Google Scholar 

  • Diamandas A, Razon MR, Ramirez-Arcos S, Brassinga AKC (2021) The virulence of S marcescens strains isolated from contaminated blood roducts is divergent in the C. elegans infection model. Front Genet 12:667062. https://doi.org/10.3389/fgene.2021.667062

    Article  CAS  Google Scholar 

  • Diao G, Wang Y, Wang C, Yang C (2011) Cloning and Functional Characterization of a Novel Glutathione S-Transferase Gene from Limonium bicolor. Plant Mol Biol Rep 29:77–87

    Article  CAS  Google Scholar 

  • Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signalling. Physiol Plant 100:241–254

    Article  CAS  Google Scholar 

  • Głowacka K, Źróbek-Sokolnik A, Okorski A, Najdzion J (2019) The effect of cadmium on the activity of stress-related enzymes and the ultrastructure of pea roots. Plants (basel, Switzerland) 8(10):413. https://doi.org/10.3390/plants8100413

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    Article  CAS  Google Scholar 

  • Hameed A, Sheikh MA (2007) Changes in catalase, peroxidase activities and soluble proteins in wheat leaves on thiourea and H2O2 treatments. Biosci Res 4(1):21–27

    Google Scholar 

  • Hasnat A, Rahman I, Pasha M (2013) Assessment of environmental impact for tannery industries in Bangladesh. Int J Environ Sci Dev 4(2):217–220

    Article  Google Scholar 

  • Hernandez LE, Villasante CO, Montero-Palmero MB, Escobar C, Carpena RO (2012) Heavy metal perception in a microscale environment: a model system using high doses of pollutants. In: Gupta DK, Sandalio LM (eds) Metal toxicity in plants: perception, signaling and remediation. Springer-Verlag, Berlin, pp 23–37. https://doi.org/10.1007/978-3-642-22081-4_2

    Chapter  Google Scholar 

  • Heshmatpure N, Rad MY (2012) The effect of PGPR (Plant-Growth-Promoting Rhizobacteria) on phytoremediation of cadmiums by canola, (Brassica napus L.) cultivars of Hyola. Ann Biol Res 2:5624–5630

    Google Scholar 

  • Huang L, Pu X, Pan JF, Wang B (2013) Heavy metal pollution status in surface sediments of Swan Lake lagoon and Rongcheng Bay in the northern Yellow Sea. Chemosphere 93(9):1957–1964

    Article  CAS  Google Scholar 

  • Igiri BE, Okoduwa SIR, Idoko GO, Akabuogu EP, Adeyi AO, Ejiogu IK (2018) Toxicity and bioremediation of heavy metals contaminated ecosystem from tannery wastewater: a review. Hindawi J Toxicol 16:2

    Google Scholar 

  • Irfan M, Ahmad A, Hayat S (2013) Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea. Saudi J Biol Sci 21:125–131

    Article  Google Scholar 

  • Khan AR, Park GS, Asaf S, Hong SJ, Jung BK, Shin JH (2017) Complete genome analysis of Serratia marcescens RSC-14: a plant growth-promoting bacterium that alleviates cadmium stress in host plants. PLoS ONE 12(2):0171534. https://doi.org/10.1371/journal.pone.0171534

    Article  CAS  Google Scholar 

  • Kotoky R, Pandey P (2019) Rhizosphere mediated biodegradation of benzo(A)pyrene by surfactin producing soil bacilli applied through Melia azadirachta rhizosphere. Int J Phytorem. https://doi.org/10.1080/15226514.2019.1663486

    Article  Google Scholar 

  • Kotoky R, Pandey P (2020) Rhizosphere assisted biodegradation of benzo(a)pyrene by cadmium resistant plant-probiotic Serratia marcescens S2I7, and its genomic traits. Sci Rep 10:5279. https://doi.org/10.1038/s41598-020-62285-4

    Article  CAS  Google Scholar 

  • Kotoky R, Pandey P (2021) The genomic attributes of Cd-resistant, hydrocarbonoclastic Bacillus subtilis SR1 for rhizodegradation of benzo(a)pyrene under co-contaminated conditions. Genomics 113(1):613–623. https://doi.org/10.1016/j.ygeno.2020.09.0577

    Article  CAS  Google Scholar 

  • Kotoky R, Singha LP, Pandey P (2017a) Draft genome sequence of polyaromatic hydrocarbon-degrading bacterium Bacillus subtilis SR1, which has plant growth-promoting attributes. Genome Announc 2:1–2

    Google Scholar 

  • Kotoky R, Singha LP, Pandey P (2017b) Draft Genome Sequence of Heavy Metal- Resistant Soil Bacterium Serratia marcescens S2I7, Which Has the Ability To Degrade Polyaromatic Hydrocarbons. Genome Announc 2:1–2

    Google Scholar 

  • Kotoky R, Nath S, Maheshwari DK, Pandey P (2019) Cadmium resistant plant growth promoting rhizobacteria Serratia marcescens S2I7 associated with the growth promotion of rice plant. Environ Sustain 2:135–144

    Article  CAS  Google Scholar 

  • Kuiper I, Bloemberg GV, Lugtenberg BJJ (2001) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol Plant-Microbe Interact 14:1197–1205

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  • Kumar V, Behl RK, Narula N (2001) Establishment of phosphate-solubilizing strains of azotobacter chroococcum in the rhizosphere and their effect on wheat cultivars under green house conditions. Microbiol Res 156 (1): 87–93 Retrieved http://www.sciencedirect.com/science/article/pii/S0944501304700142.

  • Li M, Hu CW, Zhu Q, Chen L, Kong ZM, Liu ZL (2006) Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the micro-alga Pavlova viridis (Prymnesiophyceae). Chemosphere 62:65–572

    Article  Google Scholar 

  • Li H, Liu X, Wassie M et al (2020) Selenium supplementation alleviates cadmium-induced damages in tall fescue through modulating antioxidant system, photosynthesis efficiency, and gene expression. Environ Sci Pollut Res 27:9490–9502. https://doi.org/10.1007/s11356-019-06628-3

    Article  CAS  Google Scholar 

  • Liu S, Liu H, Chen R, Ma Y, Yang B, Chen Z, Liang Y, Fang J, Xiao Y (2021) Role of two plant growth-promoting bacteria in remediating cadmium—contaminated soil combined with Miscanthus floridulus (Lab). Plants 10:912. https://doi.org/10.3390/plants10050912

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Freitas H (2009) Inoculation of plant growth promoting bacterium Achromobacter xylosoxidansstrain Ax10 for the improvement of copper phytoextraction by Brassica juncea. J Environ Manage 90:831–837

    Article  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Torgmin SA (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69(2):220–228

    Article  CAS  Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009

    Article  CAS  Google Scholar 

  • Moran MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathionereductase and glutathione-S-transferase activities in rat lung and liver. Biochim Biophys Acta 582:67–78

    Article  Google Scholar 

  • Okolo VN, Olowolafe EA, Akawu I, Okoduwa SIR (2016) Effects of industrial effluents 581 on soil resource in challawa industrial area. J Glob Ecol Environ 5(1):10

    Google Scholar 

  • Olaniran AO, Balgobind A, Pillay B (2013) Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. Int J Mol Sci 14(5):10197–10228

    Article  Google Scholar 

  • Osazee OJ, Obayagbona ON, Daniel EO (2013) Microbiological and physicochemical analyses of top soils obtained from four municipal waste dumpsites in Benin City, Nigeria. Int J Microbiol Mycol 1(1):23–30

    Google Scholar 

  • Pal AK, Sengupta C (2019) Isolation of cadmium and lead tolerant plant growth promoting rhizobacteria: Lysinibacillusvarians and Pseudomonasputida from Indian agricultural soil. Soil Sedim Contam 28(7):601–629. https://doi.org/10.1080/15320383.2019.1637398

    Article  CAS  Google Scholar 

  • Patel M, Patel K, Al-Keridis LA, Alshammari N, Badraoui R, Elasbali AM, Al-Soud WA, Hassan MI, Yadav DK, Adnan M (2022) Cadmium-tolerant plant growth-promoting bacteria Curtobacterium oceanosedimentum improves growth attributes and strengthens antioxidant system in Chili (Capsicum frutescens). Sustainability 14:4335. https://doi.org/10.3390/su14074335

    Article  CAS  Google Scholar 

  • Pena LB, Barcia RA, Azpilicueta CE, Mendez AA, Gallego SM (2012) Oxidative post translational modifications of proteins related to cell cycle are involved in cadmium toxicity in wheat seedlings. Plant Sci 196:1–7. https://doi.org/10.1016/j.plantsci.2012.07.008

    Article  CAS  Google Scholar 

  • Piacentini D, Corpas FJ, D’Angeli S, Altamura MM, Falasca G (2020) Cadmium and arsenic-induced-stress differentially modulates Arabidopsis root architecture, peroxisome distribution, enzymatic activities and their nitric oxide content. Plant Physiol Biochem 148:312–323. https://doi.org/10.1016/j.plaphy.2020.01.026

    Article  CAS  Google Scholar 

  • Prasanna BM, Vasal SK, Kassahun B, Singh NN (2001) Quality protein maize. Curr Sci 81(10):1308–1319

    CAS  Google Scholar 

  • Purkayastha GD, Mangar P, Saha A, Saha D (2018) Evaluation of the biocontrol efficacy of a Serratia marcescens strain indigenous to tea rhizosphere for the management of root rot disease in tea. PLoS ONE 13(2):e0191761. https://doi.org/10.1371/journal.pone.0191761

    Article  CAS  Google Scholar 

  • Raja C, Selvam GS, Omine K (2009) Isolation, identification and characterization of heavy metal resistant bacteria from sewage. International joint symposium on Geodisaster prevention and geo-environment in Asia JS-Fukuoka, 205–209.

  • Rajkumar M, Ma Y, Freitas H (2008) Characterization of metal-resistant plant growth promoting Bacillus weihenstephanensis isolated from serpentine soil in Portugal. J Basic Microbiol 48:1–9

    Article  Google Scholar 

  • Rajkumari J, Choudhury Y, Bhattacharjee K, Pandey P (2021) Rhizodegradation of pyrene by a non-pathogenic klebsiella pneumoniae isolate applied with tagetes erecta l and changes in the rhizobacterial community. Front Microbiol 12:593023. https://doi.org/10.3389/fmicb.2021.593023

    Article  Google Scholar 

  • Reed MLE, Glick BR (2005) Growth of canola (Brassica napus) in the presence of plant growth-promoting bacteria and either copper or polycyclic aromatic hydrocarbons. Can J Microbiol 51(12):1061–1069

    Article  CAS  Google Scholar 

  • Rehman M, Liua L, Bashirb S, Saleema MH, Chena C, Penga D, Siddiquec KHM (2019) Influence of rice straw biochar on growth, antioxidant capacity and copper uptake in ramie (Boehmeria nivea L.) grown as forage in aged copper contaminated soil. Plant Physiol Biochem 138:121–129

    Article  CAS  Google Scholar 

  • Rizvi A, Khan MS (2018) Heavy metal induced oxidative damage and root morphology alterations of maize (Zea mays L.) plants and stress mitigation by metal tolerant nitrogen fixing Azotobacter chroococcum. Ecotoxicol Environ Saf 157:9–20

    Article  CAS  Google Scholar 

  • Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23(18):17859–17879

    Article  CAS  Google Scholar 

  • Romdhane L, Panozzo A, Radhouane L, Dal Cortivo C, Barion G, Vamerali T (2021) Characteristics and metal uptake of maize (Zea mays L.) under xtreme soil contamination. Agronomy 11:178. https://doi.org/10.3390/agronomy11010178

    Article  CAS  Google Scholar 

  • Saha J, Sarkar M, Mandal P, Pal A (2022) Comparative study of heavy metal uptake and analysis of plant growth promotion potential of multiple heavy metal-resistant bacteria isolated from arable land. Curr Microbiol 79:7

    Article  CAS  Google Scholar 

  • Schulenburg H, Ewbank JJ (2004) Diversity and specificity in the interaction between Caenorhabditis elegans and the pathogen Serratia marcescens. BMC Evol Biol 2004(4):49. https://doi.org/10.1186/1471-2148-4-49

    Article  CAS  Google Scholar 

  • Shahzad A, Qin M, Elahie M, Naeem M, Bashir T, Yasmin H, Younas M, Areeb A, Irfan M, Billah M, Shakoor A, Zulfiqar S (2021) Bacillus pumilus induced tolerance of Maize (Zea mays L.) against Cadmium (Cd) stress. Sci Rep 11:17196. https://doi.org/10.1038/s41598-021-96786-7

    Article  CAS  Google Scholar 

  • Sheng XF, Xia JJ (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64:1036–1042

    Article  CAS  Google Scholar 

  • Singh VP, Singh S, Kumar J, Prasad SM (2015) Investigating the roles of ascorbate-glutathione cycle and thiol metabolism in arsenate tolerance in ridged Luffa seedlings. Protoplasma 252:1217–1229. https://doi.org/10.1007/s00709-014-0753-6

    Article  CAS  Google Scholar 

  • Singh HN, Jayashree R, Narayan SL (2018) Heavy metal occurrence in the soil of high input tea agroecosystem of Southern Assam, Northeast India, Vegetos. Int J Plant Res 31(3):47–54. https://doi.org/10.5958/2229-4473.2018.00072.1

    Article  Google Scholar 

  • Singha P, Pandey P (2017) Glutathione and glutathione-S-transferase activity in Jatropha curcas in association with pyrene degrader Pseudomonas aeruginosa PDB1 in rhizosphere, for alleviation of stress induced by polyaromatic hydrocarbon for effective rhizoremediation L. Ecol Eng 102:422–432

    Article  Google Scholar 

  • Singha LP, Pandey P (2021) Rhizosphere assisted bioengineering approaches for the mitigation of etroleum hydrocarbons contamination in soil. Crit Rev Biotechnol. https://doi.org/10.1080/07388551.2021.1888066

    Article  Google Scholar 

  • Thakare M, Sarma H, Datar S, Roy A, Pawar P, Gupta K, Pandit S, Prasad R (2021) Understanding the holistic approach to plant-microbe remediation technologies for removing heavy metals and radionuclides from soil. Curr Res Biotechnol 3:84–98

    Article  CAS  Google Scholar 

  • Toth G, Hermann T, Da Silva MR, Montanarella L (2016) Heavy metals in agricultural soils of the European Union with implications for food safety. Environ Int 88:299–309

    Article  CAS  Google Scholar 

  • Van Assche F, Clijsters H (1990) Effects of metals on enzyme in plants. Plant Cell Environ 13:195–206

    Article  Google Scholar 

  • Xu X, Cao X, Zhao L, Wang H, Yu H, Gao B (2013) Removal of Cu, Zn, and Cd from aqueous solutions by the dairy manure-derived biochar. Environ Sci Pollut Res 20:358–368

    Article  CAS  Google Scholar 

  • Yaouba A, Tatsadjieu N, Jazet DP, Mbofung CM (2012) Inhibition of fungal development in maize grains under storage condition by essential oils. Int J Biosci 2(6):41–48

    Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64(6):991–997

    Article  CAS  Google Scholar 

  • Zhang L, Chang X, Li Z, He Q (2010) Selective solid-phase extraction using oxidized activated carbon modified with triethylenetetramine for preconcentration of metal ions. J Mol Struct 964:58–62

    Article  CAS  Google Scholar 

  • Zhou L, Zhang L, He Y, Liu F, Li M, Wang Z, Ji G (2014) Isolation and characterization of bacterial isolates for biological control of clubroot on Chinese cabbage. Eur J Plant Pathol 140:159–168. https://doi.org/10.1007/s10658-014-0451-4

    Article  CAS  Google Scholar 

Download references

Acknowledgements

BB and PP acknowledge the Department of Biotechnology (DBT), Govt. of India for financial support, RK acknowledges the Department of Science and Technology (DST), Govt. of India for DST-INSPIRE fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Piyush Pandey.

Ethics declarations

Competing interests

Authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 123 KB)

Rights and permissions

Springer Nature or its licensor 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhuyan, B., Kotoky, R., Maheshwari, D.K. et al. Rhizoremediation of Cd-contaminated soil using Zea mays Sturt, with heavy metal resistant rhizobacteria that alleviate Cd-induced stress in plant. Environmental Sustainability 5, 375–387 (2022). https://doi.org/10.1007/s42398-022-00241-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42398-022-00241-w

Keywords

Navigation