Skip to main content
Log in

Enhanced uptake of Cd, Cr, and Cu in Catharanthus roseus (L.) G.Don by Bacillus cereus: application of moss and compost to reduce metal availability

  • Environmental Toxicology and Risks Associated with Human Health
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Heavy metals (HMs) being the notorious and toxic are being introduced into the environment credited to natural and anthropogenic activities. The use of ornamental plants is being ignored as potential candidates for HMs phytoremediation. In this study, pot experiments were conducted on Catharanthus roseus (L.) G.Don to evaluate selected heavy metals tolerance and accumulation potential with reference to the bacterial endophyte (Bacillus cereus) and organic amendments (moss and compost at 5% v/v). Results indicated improvement in uptake of Cd (230 mg kg−1), Cu (229 mg kg−1), and Cr (458 mg kg−1) by C. roseus with B. cereus. The concentration of Ni and Pb was found highest in controls (without strain) that were 420 and 904 mg kg−1, respectively. Conversely, the addition of organic amendments enhanced biomass production, as compared to controls, 441, 471, and 763% by peat moss (T3), compost (T4), and peat moss + compost + inoculum treatments (T6), respectively, while reduction of plant HMs content was observed. Microbial-aided phytoremediation/phytoextraction could be a potential method for removal of Cd, Cr, and Cu, while organic amendments can significantly improve plant growth in the presence of heavy metals.

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
Fig. 7

Similar content being viewed by others

References

  • Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles and fate of organic acids in soils: a review. S Afr J Bot 108:393–406

    CAS  Google Scholar 

  • Anjum F, Bhatti HN, Asgher M, Shahid M (2010) Leaching of metal ions from black shale by organic acids produced by Aspergillus niger. Applied Clay Science 47:356–361

  • Arab F, Mulligan CN (2018) An eco-friendly method for heavy metal removal from mine tailings. Environ Sci Pollut Res Int 25:16202–16216

    CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1

    CAS  Google Scholar 

  • Arshad M, Khan AHA, Hussain H, Anees M, Iqbal M, Soja G, Yousaf S (2017) The reduction of chromium (VI) phytotoxicity and phytoavailability to wheat (Triticum aestivum L.) using biochar and bacteria. Appl Soil Ecol 114:90–98

    Google Scholar 

  • Beesley L, Marmiroli M (2011) The immobilisation and retention of soluble arsenic, cadmium and zinc by biochar. Environ Pollut 159:474–480

    CAS  Google Scholar 

  • Bidar G, Pelfrêne A, Louvel B, Janus A, Douay F (2019) Influence of amendments on metal environmental and toxicological availability in highly contaminated brownfield and agricultural soils. Environ Sci Pollut Res 26:33086–33108

    CAS  Google Scholar 

  • Boechat CL, Giovanella P, Amorim MB, de Sa ELS, de Oliveira Camargo FA (2017) Metal-resistant rhizobacteria isolates improve Mucuna deeringiana phytoextraction capacity in multi-metal contaminated soils from a gold mining area. Environ Sci Pollut Res 24:3063–3073

    CAS  Google Scholar 

  • Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286

    Google Scholar 

  • Budak F, Zaimoglu Z, Bascı N (2011) Uptake and translocation of hexavalent chromium by selected species of ornamental plants. Pol J Environ Stud 20:857–862

    CAS  Google Scholar 

  • Cui S, Zhang T, Zhao S, Li P, Zhou Q, Zhang Q, Han Q (2013) Evaluation of three ornamental plants for phytoremediation of Pb-contaminated soil. Int J Phytoremediat 15:299–306

    CAS  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    CAS  Google Scholar 

  • Dodangeh H, Rahimi G, Fallah M, Ebrahimi E (2018) Investigation of heavy metal uptake by three types of ornamental plants as affected by application of organic and chemical fertilizers in contaminated soils. Environ Earth Sci 77:473

    Google Scholar 

  • Estefan G, Sommer R, Ryan J (2013) Methods of soil, plant, and water analysis. A manual for the West Asia and North Africa region 3

  • Farrell M, Perkins WT, Hobbs PJ, Griffith GW, Jones DL (2010) Migration of heavy metals in soil as influenced by compost amendments. Environ Pollut 158:55–64

    CAS  Google Scholar 

  • Forte J, Mutiti S (2017) Phytoremediation potential of Helianthus annuus and Hydrangea paniculata in copper and lead-contaminated soil. Water Air Soil Pollut 228:77

    Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    CAS  Google Scholar 

  • Han-Song C, Qiao-Yun H, Li-Na L, Peng C, Wei L, Ming L (2010) Poultry manure compost alleviates the phytotoxicity of soil cadmium: influence on growth of Pakchoi (Brassica chinensis L.). Pedosphere 20:63–70

  • Hussain F, Hussain I, Khan AHA, Muhammad YS, Iqbal M, Soja G, Yousaf S (2018) Combined application of biochar, compost, and bacterial consortia with Italian ryegrass enhanced phytoremediation of petroleum hydrocarbon contaminated soil. Environ Exp Bot 153:80–88

    CAS  Google Scholar 

  • Iqbal M, Nawaz I, Hassan Z, Hakvoort HW, Bliek M, Aarts MG, Schat H (2013) Expression of HMA4 cDNAs of the zinc hyperaccumulator Noccaea caerulescens from endogenous NcHMA4 promoters does not complement the zinc-deficiency phenotype of the Arabidopsis thaliana hma2hma4 double mutant. Front Plant Sci 4:404

    Google Scholar 

  • Iqbal A, Mushtaq MU, Khan AHA, Nawaz I, Yousaf S, Iqbal M (2019) Influence of Pseudomonas japonica and organic amendments on the growth and metal tolerance of Celosia argentea L. Environ Sci Pollut Res Int 2019:1–15

    Google Scholar 

  • Jones S, Bardos RP, Kidd PS, Mench M, de Leij F, Hutchings T, Herzig R (2016) Biochar and compost amendments enhance copper immobilisation and support plant growth in contaminated soils. J Environ Manag 171:101–112

    CAS  Google Scholar 

  • Khan AHA, Tanveer S, Alia S, Anees M, Sultan A, Iqbal M, Yousaf S (2017a) Role of nutrients in bacterial biosurfactant production and effect of biosurfactant production on petroleum hydrocarbon biodegradation. Ecol Eng 104:158–164

    Google Scholar 

  • Khan WU, Ahmad SR, Yasin NA, Ali A, Ahmad A (2017b) Effect of Pseudomonas fluorescens RB4 and Bacillus subtilis 189 on the phytoremediation potential of Catharanthus roseus (L.) in Cu and Pb-contaminated soils. Int J Phytoremediat 19:514–521

    Google Scholar 

  • Khan AHA, Butt TA, Mirza CR, Yousaf S, Nawaz I, Iqbal M (2019a) Combined application of selected heavy metals and EDTA reduced the growth of Petunia hybrida L. Sci Rep 9:4138

    Google Scholar 

  • Khan AHA, Nawaz I, Yousaf S, Cheema AS, Iqbal M (2019b) Soil amendments enhanced the growth of Nicotiana alata L. and Petunia hydrida L. by stabilizing heavy metals from wastewater. J Environ Manag 242:46–55

    CAS  Google Scholar 

  • Khan AHA, Nawaz I, Qu Z, Butt TA, Yousaf S, Iqbal M (2020) Reduced growth response of ornamental plant Nicotiana alata L. upon selected heavy metals uptake, with co-application of ethylenediaminetetraacetic acid. Chemosphere 241:125006

    CAS  Google Scholar 

  • Kong Z, Glick BR (2017) The role of plant growth-promoting bacteria in metal phytoremediation. Adv Microb Physiol 71:97–132

    CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    CAS  Google Scholar 

  • Liu J-n, Q-x Z, Sun T, Ma LQ, Wang S (2008) Growth responses of three ornamental plants to Cd and Cd–Pb stress and their metal accumulation characteristics. J Hazard Mater 151:261–267

    CAS  Google Scholar 

  • Liu J, Xin X, Zhou Q (2018) Phytoremediation of contaminated soils using ornamental plants. Environ Rev 26:43–54

    CAS  Google Scholar 

  • Ma Y, Oliveira RS, Wu L, Luo Y, Rajkumar M, Rocha I, Freitas H (2015) Inoculation with metal-mobilizing plant-growth-promoting rhizobacterium Bacillus sp. SC2b and its role in rhizoremediation. J Toxic Environ Health A 78:931–944

    CAS  Google Scholar 

  • Man YB, Chung AKC, Wong MH (2016) Changes in low molecular weight organic acids and antioxidative enzyme activities of wetland plants under metal stresses. Environ Eng Manag J 15:1657–1663

    CAS  Google Scholar 

  • McBride MB, Shayler HA, Russell-anelli JM, Spliethoff HM, Marquez-bravo LG (2015) Arsenic and lead uptake by vegetable crops grown on an old orchard site amended with compost. Water Air Soil Pollut 226:1–10

    CAS  Google Scholar 

  • Nwachukwu OI, Pulford ID (2008) Comparative effectiveness of selected adsorbant materials as potential amendments for the remediation of lead, copper and zinc-contaminated soil. Soil Use Manag 2:199–207

    Google Scholar 

  • Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197

    Google Scholar 

  • Paltseva AA, Cheng Z, Perl S, Groffman PM (2020) Remediation of an urban garden with elevated levels of soil contamination. Sci Total Environ 722:137965

    CAS  Google Scholar 

  • Prapagdee B, Wankumpha J (2017) Phytoremediation of cadmium-polluted soil by Chlorophytum laxum combined with chitosan-immobilized cadmium-resistant bacteria. Environ Sci Pollut Res Int 23:19249–19258

    Google Scholar 

  • 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 48:500–508

    CAS  Google Scholar 

  • Rajkumar M, Ma Y, Freitas H (2013) Improvement of Ni phytostabilization by inoculation of Ni resistant Bacillus megaterium SR28C. J Environ Manag 128:973–980

    CAS  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    CAS  Google Scholar 

  • Raza A, Khan AHA, Nawaz I, Qu Z, Yousaf S, Ali MA, Iqbal M (2019) Evaluation of arsenic-induced stress in Dahlia pinnata Cav.: morphological and physiological response. Soil Sediment Contam 28:716–728

    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 23:17859–17879

  • Semenya SS, Potgieter MJ (2013) Catharanthus roseus (L.) G.Don.: extraordinary Bapedi medicinal herb for gonorrhoea. J Med Plant Res 7:1434–1438

    Google Scholar 

  • Stanislawska-Glubiak E, Korzeniowska J, Kocon A (2015) Effect of peat on the accumulation and translocation of heavy metals by maize grown in contaminated soils. Environ Sci Pollut Res Int 22:4706–4714

    CAS  Google Scholar 

  • Tejada M, Benítez C (2015) Application of vermicomposts and compost on tomato growth in greenhouses. Compost Sci Util 23:94–103

    CAS  Google Scholar 

  • Tordoff G, Baker A, Willis A (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228

    CAS  Google Scholar 

  • Touceda-González M, Brader G, Antonielli L, Ravindran VB, Waldner G, Friesl-Hanl W, Sessitsch A (2015) Combined amendment of immobilizers and the plant growth-promoting strain Burkholderia phytofirmans PsJN favours plant growth and reduces heavy metal uptake. Soil Biol Biochem 91:140–150

    Google Scholar 

  • Yang Z, Liu L, Lv Y, Cheng Z, Xu X, Xian J, Zhu X, Yong Y (2018) Metal availability, soil nutrients, and enzyme activity in response to application of organic amendments in Cd-contaminated soil. Environ Sci Pollut Res Int 22:2425–2435

    Google Scholar 

Download references

Funding

The present study was financially supported by the specialized University Research Funds (URF) of Quaid-i-Azam University (QAU), Islamabad.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Aqib Hassan Ali Khan or Mazhar Iqbal.

Ethics declarations

Conflict of interest

The authors declare no competing or conflict of interest.

Additional information

Responsible Editor: Elena Maestri

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 24 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mushtaq, M.U., Iqbal, A., Nawaz, I. et al. Enhanced uptake of Cd, Cr, and Cu in Catharanthus roseus (L.) G.Don by Bacillus cereus: application of moss and compost to reduce metal availability. Environ Sci Pollut Res 27, 39807–39818 (2020). https://doi.org/10.1007/s11356-020-08839-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-08839-5

Keywords

Navigation