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Optimization of Copper (II) Removal by Response Surface Methodology Using Root Nodule Endophytic Bacteria Isolated from Vigna unguiculata

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Abstract

The present study was conducted to investigate copper tolerance and bioremediation potential in endophytic bacteria isolated from Vigna unguiculata root nodules. Total ten endophytes were isolated on yeast mannitol agar and enriched in copper (II) sulfate (CuSO4) up to 500 mg/L. Four endophytes belonging to genera Bacillus and Arthrobacter showed copper tolerance. The isolates were identified as Arthrobacter tumbae MYR1, Bacillus safensis MYR2, Bacillus pumilus MYR3 and Bacillus sp. MYR4 using 16S ribosomal RNA (rRNA) analysis. Response surface methodology was used for copper (II) removal optimization. The model was significant with R 2, P and F value of 0.9780, <0.0001, and 34.54, respectively. Results showed that highest copper (II) bioremoval of 82.8 % was obtained at pH 5.0, temperature 32.5 °C, and 600 mg/L copper concentration after 168 h of incubation. The isolates were tested for plant growth promotion and all the strains produced indole acetic acid (IAA) and showed 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase activity. The study concludes that endophytic bacteria possessed greater potential for copper tolerance and bioremediation.

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References

  • Amini, M., Younesi, H., Bahramifar, N., Lorestani, A. A., Ghorbani, F., Daneshi, A., Sharifzadeh, M., (2008). Application of response surface methodology for optimization of lead biosorption in an aqueous solution by Aspergillus niger. Journal of Hazardous Material, 154, 694–702.

  • Andreazza, R., Pieniz, S., Okeke, B. C., & Camargo, F. A. O. (2011). Evaluation of copper resistant bacteria from vineyard soils and mining waste for copper biosorption. Brazilian Journal of Microbiology, 42(1), 66–74.

    Article  CAS  Google Scholar 

  • Ashikuzzaman, M., Shahriyar, S., Lijon, M. B., Rahman, M. A., Hassan, M. M., & Asif, A. A. (2015). An investigation on heavy metal tolerance properties of bacteria isolated from textile effluent. Journal of Biodiversity and Environmental Sciences, 7(6), 62–71.

    Google Scholar 

  • Babu, A. G., Kim, J., & Oh, B. (2013). Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. Journal of Hazardous Materials, 250, 477–483.

    Article  Google Scholar 

  • Bafana, A., Krishnamurthi, K., Patil, M., & Chakrabarti, T. (2010). Heavy metal resistance in Arthrobacter ramosus strain G2 isolated from mercuric salt-contaminated soil. Journal of Hazardous Materials, 177(1–3), 481–6.

    Article  CAS  Google Scholar 

  • Baltazar, M., Gracioso, L., Avanzi, I., Veiga, M., Gimenes, L., Nascimento, C., & Perpetuo, E. (2014). Bioremediation potential of Pseudomonas aeruginosa and Enterobacter cloacae isolated from a copper-contaminated area. BMC Proceedings, 8(Suppl 4), 188.

    Article  Google Scholar 

  • Bestawy, E. E., Helmy, S., Hussien, H., Fahmy, M., Amer, R. (2013). Bioremediation of heavy metal-contaminated effluent using optimized activated sludge bacteria. Applied water science, 3(1), 181–192.

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of dye binding. Analytic Biochemistry, 72, 248–254.

    Article  CAS  Google Scholar 

  • Chen, X. C., Wang, Y. P., Lin, Q., Shi, J. Y., Wu, W. X., & Chen, Y. X. (2005). Biosorption of copper (II) and zinc (II) from aqueous solution by Pseudomonas putida CZ1. Colloids and Surfaces B: Biointerfaces, 46, 101–107.

    Article  CAS  Google Scholar 

  • Congeevarama, S., Dhanarani, S., Park, J., Dexilin, M., & Thamaraiselvi, K. (2007). Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. Journal of Hazardous Materials, 146, 270–277.

    Article  Google Scholar 

  • Davis, J. A., Volesky, B., & Vierra, R. H. S. F. (2000). Sargassum seaweed as biosorbent for heavy metals. Water Research, 34(17), 4270–4278.

    Article  CAS  Google Scholar 

  • Dey, S., & Paul, A. K. (2015). Hexavalent chromate reduction during growth and by immobilized cells of Arthrobacter sp. SUK 1205. Science, Technology and Development, 34(3), 158–168.

    Article  Google Scholar 

  • Dworkin, M., & Foster, J. W. (1958). Experiments with some microorganisms which utilize ethane and hydrogen. Journal of Bacteriology, 75, 592–603.

    CAS  Google Scholar 

  • Fang, L., Yang, S., Huang, Q., Xue, A., & Cai, P. (2014). Biosorption mechanisms of Cu (II) by extracellular polymeric substances from Bacillus subtilis. Chemical Geology, 386, 143–151.

    Article  CAS  Google Scholar 

  • Feris, K., Ramsey, P., Frazar, C., Moore, J. N., Gannon, J. E., & Holbert, W. E. (2003). Differences in hyporheic-zone microbial community structure along a heavy-metal contamination gradient. Applied and Environmental Microbiology, 69, 5563–5573.

    Article  CAS  Google Scholar 

  • Galun, M. E., Galun, E., Siegel, B. Z., Keller, P., Lehr, H., & Siegel, S. M. (1987). Removal of metal ions from aqueous solutions by Penicillium biomass: kinetic and uptake parameters. Water, Air, and Soil Pollution, 33, 359–371.

    Article  CAS  Google Scholar 

  • Ghosh, A., & Saha, P. D. (2013a). Optimization of copper bioremediation by Stenotrophomonas maltophilia PD2. Journal of Environmental Chemical Engineering, 1(3), 159–163.

    Article  CAS  Google Scholar 

  • Ghosh, A., & Saha, P. D. (2013b). Optimization of copper reduction from solution using Bacillus pumilus PD3 isolated from marine water. Elixir Pollution, 55, 12910–12914.

    Google Scholar 

  • Goksungur, Y., Uren, S., & Guvenc, U. (2003). Biosorption of copper ions by caustic treated waste baker’s yeast biomass. Turkish Journal of Biology, 27, 23–29.

    CAS  Google Scholar 

  • Gordon, S. A., & Weber, R. P. (1951). Colorimetric estimation of indole acetic acid. Plant Physiology, 26, 192–195.

    Article  CAS  Google Scholar 

  • Guo, H., Luo, S., Chen, L., Xiao, X., Xi, Q., Wei, W., Zeng, G., Liu, C., Wan, Y., Chen, J., & He, Y. (2010). Bioremediation of heavy metals by growing hyper accumulator endophytic bacterium Bacillus sp. L14. Bioresource Technology, 101, 8599–8605.

    Article  CAS  Google Scholar 

  • Jafari, S. A., Cheraghi, S., Mirbakhsh, M. (2015). Isolation of mercury-resistant bacteria from Bushehr Coastal sediments and optimization of soluble mercury bioremediation by RSM. 1st International and 9th National Biotechnology Congress of Islamic Republic of Iran, Tehran.

  • Kumar, V., Singh, S., Kashyap, N., Singla, S., Bhadrecha, P., Kaur, P., Datta, S., Kalia, A., & Singh, J. (2015). Bioremediation of heavy metals by employing resistant microbial isolates from agricultural soil irrigated with industrial waste water. Oriental Journal of Chemistry, 31(1), 357–361.

    Article  Google Scholar 

  • Long, X., Chen, X., Chen, Y., Woon-Chung, W. J., Wei, Z., & Wu, Q. (2011). Isolation and characterization endophytic bacteria from hyperaccumulator Sedum alfredii Hance and their potential to promote phytoextraction of zinc polluted soil. World Journal of Microbiology and Biotechnology, 27, 1197–1207.

    Article  CAS  Google Scholar 

  • Lovley, D. R. (1995). Bioremediation of organic and metal contaminants with dissimilatory metal reduction. Journal of Industrial Microbiology and Biotechnology, 14, 85–93.

    Article  CAS  Google Scholar 

  • Ma, Y., Rajkumar, M., & Freitas, H. (2009). Improvement of plant growth and nickel uptake by nickel resistant-plant growth promoting bacteria. Journal of Hazardous Materials, 166(2–3), 1154–1161.

    Article  CAS  Google Scholar 

  • Ma, Y., Oliveira, R. S., Nai, F., Rajkumar, M., Luo, Y., Rocha, I., & Freitas, H. (2015). The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. Journal of Environmental Management, 156, 62–69.

    Article  CAS  Google Scholar 

  • Nagata, S., Yamaji, K., Nomura, N., & Ishimoto, H. (2015). Root endophytes enhance stress-tolerance of Cicuta virosa L. growing in a mining pond of eastern Japan. Plant Species Biology, 30(2), 116–125.

    Article  Google Scholar 

  • Nonnoi, F., Chinnaswamy, A., de la Torre, V. S. G., de la Pẽna, T. C., Lucas, M. M., Pueyo, J. J. (2012). Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago  spp. and Trifolium spp.) growing in mercury-contaminated soils. Applied Soil Ecology, 61, 49–59.

  • Patten, C. L., & Glick, B. R. (2002). Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Applied and Environmental Microbiology, 68, 3795–3801.

    Article  CAS  Google Scholar 

  • Petrini, O. (1991). Fungal endophytes of tree leaves. In J. Andrews & Hirano (Eds.), Microbial ecology of leaves (pp. 179–197). New York: Springer.

    Chapter  Google Scholar 

  • Płociniczaka, T., Sinkkonenb, A., Romantschukb, M., & Piotrowska-Sege, Z. (2013). Characterization of Enterobacter intermedius MH8b and its use for the enhancement of heavy metals uptake by Sinapis alba L. Applied Soil Ecology, 63, 1–7.

    Article  Google Scholar 

  • Rajeshkumar, R., & Kartic, N. (2011). Removal of Cu2+ ions from aqueous solutions using copper resistant bacteria. Our Nature, 9, 49–54.

    Google Scholar 

  • Rajeshkumar, R., Shankar, C., & Thamaraiselvi, K. (2011). Evaluation of isolated fungal strain from e-waste recycling facility for effective sorption of toxic heavy metal Pb (II) ions and fungal protein molecular characterization—a mycoremediation approach. Asian Journal of Experimental Biological Sciences, 2, 342–347.

    Google Scholar 

  • Rajkumar, M., Ma, Y., & Freitas, H. (2008). Characterization of metal-resistant plant-growth promoting Bacillus weihenstephanensis isolated from serpentine soil in Portugal. Journal of Basic Microbiology, 48, 500–508.

    Article  CAS  Google Scholar 

  • Rathaur, P., Ramteke, P. W., Raja, W., & John, S. A. (2012). Isolation and characterization of nickel and cadmium tolerant plant growth promoting rhizobacteria from rhizosphere of Withania somnifera. Journal of Biodiversity and Environmental Sciences, 6(18), 253–261.

    Google Scholar 

  • Schwyn, B., Neilands, J. (1987). Universal chemical assay for the detection and determination of siderophores. Analytic Chemistry, 160, 47–56.

  • Shin, M. N., Shim, J., You, Y., Myung, H., Bang, K. S., Cho, M., Kamala-Kannan, S., & Oh, B. T. (2012). Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma. Journal of Hazardous Materials, 199, 314–320.

    Article  Google Scholar 

  • Tapiero, H., Townsend, H. D. M., & Tew, K. D. (2003). Trace elements in human physiology and pathology. Copper, Biomedicine and Pharmacotherapy, 57, 386–398.

    Article  CAS  Google Scholar 

  • Vincent, J. M. (1970). A manual for the practical study of root nodule bacteria. Oxford: Black-well.

    Google Scholar 

  • Zaidi, S., Usmani, S., Singh, B. R., & 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, 991–997.

    Article  CAS  Google Scholar 

  • Zhang, Y. F., He, L. Y., Chen, Z. J., Wang, Q. Y., Qian, M., & Sheng, X. F. (2011). Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere, 83, 57–62.

    Article  CAS  Google Scholar 

  • Zhang, W., Huang, Z., He, L., & Sheng, X. (2012). Assessment of bacterial communities and characterization of lead-resistant bacteria in the rhizosphere soils of metal-tolerant Chenopodium ambrosioides grown on lead–zinc mine tailings. Chemosphere, 87(10), 1171–1178.

    Article  CAS  Google Scholar 

  • Zhao, L., Xu, Y., Sun, R., Deng, Z., Yang, W., & Wei, G. (2011). Identification and characterization of the endophytic plant growth prompter Bacillus cereus strain mq23 isolated from Sophora alopecuroides root nodules. Brazilian Journal of Microbiology, 42, 567–575.

    Article  Google Scholar 

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Authors and Affiliations

  1. Research Scholar, Centre for Environmental Science and Technology, School of Environment and Earth Sciences, Central University of Punjab, Bathinda, 151001, India

    R. Manohari

  2. Centre for Environmental Science and Technology, School of Environment and Earth Sciences, Central University of Punjab, Bathinda, 151001, India

    K. N. Yogalakshmi

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  1. R. Manohari
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Correspondence to K. N. Yogalakshmi.

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Manohari, R., Yogalakshmi, K.N. Optimization of Copper (II) Removal by Response Surface Methodology Using Root Nodule Endophytic Bacteria Isolated from Vigna unguiculata . Water Air Soil Pollut 227, 285 (2016). https://doi.org/10.1007/s11270-016-2964-2

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