Skip to main content
Log in

Antioxidants and chromium reductases by Penibacillus species enhance the growth of soybean under chromium stress

  • Original Paper
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

Hexavalent chromium [Cr(VI)] is used in various industries, but its improper and uncontrolled discharge contaminates the environment. In order to circumvent chromium toxicity, several physicochemical and biological strategies have been employed. Among biological approach, microbes convert toxic Cr(VI) to less soluble Cr(III) form and hence can be used to detoxify/remove Cr(VI) from contaminated environment. Considering these, present study was designed to assess the effect of chromium reductases and antioxidants secreted by Penibacillus species to detoxify Cr(VI) and concurrently to augment soybean growth. Bacterial strains (MAI1 and MAI2) were identified as Penibacillus sp. using 16S rRNA gene. Penibacillus species reduced Cr(VI) significantly at pH 7. Maximum Cr(VI) was reduced at 50 and 100 µg/ml of Cr(VI) concentrations. Penibacillus sp. also reduced Cr(VI) significantly at 25 and 35 °C as well as 1 g sodium alginate in 1 g polyvinyl alcohol. Bacterial strains reduced Cr(VI) into Cr(III) which were detected as 33 ± 1 and 35 ± 1 µg/ml in supernatant and 67 ± 2.5 and 65 ± 1 µg/ml in cell debris, respectively, after 120 h. Chromium reductase found in cell-free extract reduced almost all Cr(VI) compared to those observed in cell debris. Both malondialdehyde and antioxidant levels were increased with gradual increase in Cr(VI) concentration. Penibacillus species inoculated soybean plants had better growth and photosynthetic pigments under Cr(VI) stress.

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

References

  • Ackerley DF, Gonzalez CF, Park CH, Blake R, Keyhan M, Matin A (2004) Chromate-reducing properties of soluble flavoproteins from Pseudomonas putida and Escherichia coli. Appl Environ Microbio 70(2):873–882

    Article  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplats, polyphenol oxidase in Beta vulgaris. Plant Physiol 25:1–15

    Article  Google Scholar 

  • Azcon R, Peralvarez MC, Biro B, Antonio Roldan A, Ruız-Lozano JM (2009) Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multicontaminated soil amended with treated lignocellulosic agrowaste. Appl Soil Ecol 41:168–177

    Article  Google Scholar 

  • Bahafid W, Joutey NT, Sayel H, Ghachtouli NE (2013) Mechanism of hexavalent chromium detoxification using Cyberlindnera fabianii yeast isolated from contaminated site in Fez (Morocco). J Mater Environ Sci 4(6):840–847

    CAS  Google Scholar 

  • Batayneh AT (2012) Toxic (aluminum, beryllium, boron, chromium and zinc) in groundwater: health risk assessment. Int J Environ Sci Technol 9:153–162

    Article  CAS  Google Scholar 

  • Batool R, Qurrat-ul-ain K, Naeem A (2014) Comparative study of Cr(VI) removal by Exiguobacterium sp. in free and immobilized forms. Bioremediation J 18:317–327

    Article  CAS  Google Scholar 

  • Batool R, Yrjala K, Hasnain S (2015) Alleviation of phyto-toxic effects of chromium by inoculation of chromium (VI) reducing Pseudomonas aeruginosa Rb-1 and Ochrobactrum intermedium Rb-2. Int J Agric Biol 17:21–30

    CAS  Google Scholar 

  • Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-Vogel M et al (2008) Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl Environ Microbiol 74:3718–3729

    Article  CAS  Google Scholar 

  • Conesa HM, Evangelou MWH, Robinson BH, Schulin R (2012) A critical view of current state of phytotechnologies to remediate soils: still a promising tool? Sci World J. doi:10.1100/2012/173829

    Article  Google Scholar 

  • Das S, Mishra J, Das SK, Pandey S, Rao DS, Chakraborty A, Sudarshan M, Das N, Thatoi H (2014) Investigation on mechanism of Cr(VI) reduction and removal by Bacillus amyloliquefaciens, a novel chromate tolerant bacterium isolated from chromite mine soil. Chesosphere 96:112–121

    Article  CAS  Google Scholar 

  • DeFilippi LJ, Lupton FS (1992) Bioremediation of soluble Cr(VI) using sulfate reducing bacteria. In: Allied signal research, national R and B conference on the control of hazardous materials, San Francisco

  • Desai C, Jain K, Madamwar D (2008a) Evaluation of In vitro Cr(VI) reduction potential in cytosolic extracts of three indigenous Bacillus sp. Isolated from Cr(VI) polluted industrial landfill. Biores Technol 99:6059–6069

    Article  CAS  Google Scholar 

  • Desai C, Jain K, Madamwar D (2008b) Hexavalent chromate reductase activity in cytosolic of Pseudomonas sp. G1DM21 isolated from Cr(VI) contaminated industrial landfill. Proc Biochem 43:713–721

    Article  CAS  Google Scholar 

  • Dhal B, Thatoi HN, Das NN, Pandey BD (2010) Reduction of hexavalent chromium by Bacillus sp. isolated from chromite mine soils and characterization of reduced product. J Chem Technol Biotechnol 85:1471–1479

    CAS  Google Scholar 

  • Eaton AD, Clesceri LS, Greenberg AE (1992) Standard methods for the examination of water and wastewater, American Public Health Association; American Water Works Association (AWWA); Water Environment Federation (WEF), Washington DC, p 981

  • Gu Y, Xu W, Liu Y, Zeng G, Huang J, Tan X, Jian H, Hu X, Li F, Wang D (2015) Mechanism of Cr(VI) reduction by Aspergillus niger: enzymatic characteristic, oxidative stress response, and reduction product. Environ Sci Pollut Res 22:6271–6279

    Article  CAS  Google Scholar 

  • Hassan SHA, Abskharon RNN, Gad El-Rab SMF, Shoreit AAM (2008) Isolation, characterization of heavy metal resistant strain of Pseudomonas aeruginosa isolated from polluted sites in Assiut city, Egypt. J Basic Microbiol 48:168–176

    Article  CAS  Google Scholar 

  • Holt JG, Krieg NR, Sneath PHA, Staley JT, Willams ST (1994) Bergeys manual of determinative bacteriology, 9th edn. Williams and Wilkins, Philadelphia

    Google Scholar 

  • Humphries AC, Nott KP, Hall LD, Macaskie LE (2005) Reduction of Cr(VI) by immobilized cells of Desulfovibrio vulgaris NCIMB 8303 and Microbacterium sp. NCIMB 13776. Biotechnol Bioeng 90(5):589–596

    Article  CAS  Google Scholar 

  • Hussein KA, Joo JH (2013) Heavy metal resistance of bacteria and its impact on the production of antioxidant enzymes. Afr J Microbiol Res 7:2288–2296

    Article  Google Scholar 

  • Joutey NT, Sayel H, Bahafid W, Ghachtouli NE (2015) Mechanisms of hexavalent chromium resistance and removal by microorganisms. Rev Environ Contam Toxicol 233:45–69

    CAS  Google Scholar 

  • Karthik C, Oves M, Thangabalu R, Sharma R, Santhosh SB, Arulselvi PI (2016) Cellulosimicrobium funkei-like enhances the growth of Phaseolus vulgaris by modulating oxidative damage under Chromium (VI) toxicity. J Adv Res 7:839–850

    Article  CAS  Google Scholar 

  • Kathiravan MN, Karthick R, Muthu N, Muthukumar K, Velan M (2010) Sonoassisted microbial reduction of chromium. Appl Biochem Biotechnol 160:2000–2013

    Article  CAS  Google Scholar 

  • Lowry OH, Roseberough NJ, Lewis AF, Randall JR (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Mani D, Kumar C (2014) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: an overview with special reference to phytoremediation. Int J Environ Sci Technol 11:843–872

    Article  CAS  Google Scholar 

  • Mani D, Sharma B, Kumar C, Pathak N, Balak S (2012) Phytoremediation potential of helianthus annuus L in sewage irrigated indo-gangetic alluvial soils. Int J Phytoremediation 14:235–246

    Article  CAS  Google Scholar 

  • McLean JS, Beveridge TJ (2001) Chromate reduction by a Pseudomonas isolated from a site contaminated with chromated copper arsenate. Appl Environ Microbiol 67:1076–1084

    Article  CAS  Google Scholar 

  • Mishra RR, Dhal B, Dutta SK, Dangar TK, Das NN, Thatoi HN (2012) Optimization and characterization of chromium (VI) reduction in saline condition by moderately halophilic Vigribacillus sp. isolated from mangrove soil of Bhitarkanika, India. J Hazard Mater 227–228:219–226

    Article  CAS  Google Scholar 

  • Ortegel JW, Staren ED, Faber LP, Warren WH, Braun PD (2002) Modulation of tumor infiltrating lymphocyte cytolytic activity against human non small cell lung cancer. Lung Cancer 36:17–25

    Article  Google Scholar 

  • Pan X, Liu Z, Chen Z, Cheng Y, Pan D, Shao J, Lin Z, Guan X (2014) Investigation of Cr(VI) reduction and Cr(III) immobilization mechanism by planktonic cells and biofilms of Bacillus subtilis ATCC-6633. Water Res 55:19–21

    Article  CAS  Google Scholar 

  • Rai V, Vajpayee P, Singh SN, Mehrotra S (2004) Effect of chromium accumulation on photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167:1159–1169

    Article  CAS  Google Scholar 

  • Wani PA, Ayoola OH (2015) Bioreduction of Cr(VI) by heavy metal resistant Pseudomonas species. J Environ Sci Technol 8:122–130

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol. doi:10.1016/j.fct.2010.08.035

    Article  Google Scholar 

  • Wani PA, Khan MS (2013) Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull Environ Contam Toxicol 91:117–124

    Article  CAS  Google Scholar 

  • Wani PA, Omozele AB (2015) Cr(VI) Removal by Indigenous Klebsiella species PB6 isolated from contaminated soil under the influence of various factors. Curr Res Bacteriol 8(3):62–69

    Article  CAS  Google Scholar 

  • Wani PA, Omozele AB, Wasiu IA, Jamiu KO (2015a) Cr(VI) reduction by indigenous Bacillus species PB5 isolated from contaminated soil of Abeokuta, Ogun State, Nigeria. Int J Soil Sci 10:203–210

    Article  CAS  Google Scholar 

  • Wani PA, Zainab IO, Wasiu ID, Jamiu KO (2015b) Chromium (VI) reduction by Streptococcus species isolated from the industrial area of Abeokuta, Ogun State, Nigeria. Res J Microbiol 10:66–75

    Article  CAS  Google Scholar 

  • Wani PA, Olamide AN, Wasiu IA, Rafi N, Wahid S, Sunday OO (2016) Sodium alginate/polyvinyl alcohol immobilization of Brevibacillus brevis OZF6 isolated from the industrial waste water of Abeokuta, Ogun State, Nigeria and its role in the removal of toxic chromate. Brit Biotechnol J 15(1):1–10

    Article  Google Scholar 

  • Yang J, He M, Wang G (2009) Removal of toxic chromate using free and immobilized Cr(VI)-reducing bacterial cells of Intrasporangium sp. Q5-1. World J Microbiol. doi:10.1007/s11274-009-0047

    Article  Google Scholar 

  • Zhang XX, Chunjie L, Zhibiao N (2012) Effects of cadmium stress on seed germination and seedling growth of Elymus dahuricus infected with the Neotyphodium endophyte. Sci China Life Sci 55:793–799

    Article  CAS  Google Scholar 

Download references

Acknowledgements

I am specially thankful to Professor Mohammad Saghir Khan Department of Agricultural Microbiology, Faculty of Agricultural Sciences, Aligarh Muslim University Aligarh India for his tremendous efforts to correct this paper for English and scientific language.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. A. Wani.

Ethics declarations

Conflict of interest

Authors do not have any financial interest or benefit arisen from the application of this research.

Additional information

Editorial responsibility: Josef Trögl.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wani, P.A., Sunday, O.O., Kehinde, A.M. et al. Antioxidants and chromium reductases by Penibacillus species enhance the growth of soybean under chromium stress. Int. J. Environ. Sci. Technol. 15, 1531–1542 (2018). https://doi.org/10.1007/s13762-017-1533-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-017-1533-6

Keywords

Navigation