Environmental Science and Pollution Research

, Volume 25, Issue 21, pp 20486–20496 | Cite as

Removal of industrial dyes and heavy metals by Beauveria bassiana: FTIR, SEM, TEM and AFM investigations with Pb(II)

  • Deepak Gola
  • Anushree MalikEmail author
  • Maneesh Namburath
  • Shaikh Ziauddin Ahammad
Water: From Pollution to Purification


Presence of industrial dyes and heavy metal as a contaminant in environment poses a great risk to human health. In order to develop a potential technology for remediation of dyes (Reactive remazol red, Yellow 3RS, Indanthrene blue and Vat novatic grey) and heavy metal [Cu(II), Ni(II), Cd(II), Zn(II), Cr(VI) and Pb(II)] contamination, present study was performed with entomopathogenic fungi, Beauveria bassiana (MTCC no. 4580). High dye removal (88–97%) was observed during the growth of B. bassiana while removal percentage for heavy metals ranged from 58 to 75%. Further, detailed investigations were performed with Pb(II) in terms of growth kinetics, effect of process parameters and mechanism of removal. Growth rate decreased from 0.118 h−1 (control) to 0.031 h−1, showing 28% reduction in biomass at 30 mg L−1 Pb(II) with 58.4% metal removal. Maximum Pb(II) removal was observed at 30 °C, neutral pH and 30 mg L−1 initial metal concentration. FTIR analysis indicated the changes induced by Pb(II) in functional groups on biomass surface. Further, microscopic analysis (SEM and atomic force microscopy (AFM)) was performed to understand the changes in cell surface morphology of the fungal cell. SEM micrograph showed a clear deformation of fungal hyphae, whereas AFM studies proved the increase in surface roughness (RSM) in comparison to control cell. Homogenous bioaccumulation of Pb(II) inside the fungal cell was clearly depicted by TEM-high-angle annular dark field coupled with EDX. Present study provides an insight into the mechanism of Pb(II) bioremediation and strengthens the significance of using entomopathogenic fungus such as B. bassiana for metal and dye removal.


Dye Heavy metal Beauveria bassiana SEM AFM FTIR 



Vardhaman Textile Ltd., India is acknowledged for providing the industrial dyes. The authors appreciate the assistance provided by Mr. Vinod Kumar and Mr. Sabal Singh (Project staff, IIT Delhi) during the experiments. Dr. Sreedevi Upadhyayula (Department of Chemical Engineering, IIT Delhi), Dr. Deepak Varandani (Department of Physics, IIT Delhi) and Mr. D. C. Sharma (Department of Textile Engineering, IIT Delhi) are also acknowledged for their kind technical support in FTIR, AFM and SEM analyses, respectively.

Funding information

The authors gratefully acknowledge Water Technology Initiative, Department of Science and Technology [Grant no. DST/TM/WTI/2K15/167 (G)], Govt. of India for financial support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Amini M, Younesi H, Bahramifar N (2009) Biosorption of nickel(II) from aqueous solution by Aspergillus niger: response surface methodology and isotherm study. Chemosphere 75:1483–1491. CrossRefGoogle Scholar
  2. Anand P, Isar J, Saran S, Saxena RK (2006) Bioaccumulation of copper by Trichoderma viride. Bioresour Technol 97:1018–1025. CrossRefGoogle Scholar
  3. Anastasi A, Prigione V, Casieri L, Varese GC (2009) Decolourisation of model and industrial dyes by mitosporic fungi in different culture conditions. World J Microbiol Biotechnol 25:1363–1374. CrossRefGoogle Scholar
  4. Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzym Microb Technol 32:78–91. CrossRefGoogle Scholar
  5. Bhattacharya A, Dey P, Gola D et al (2015) Assessment of Yamuna and associated drains used for irrigation in rural and peri-urban settings of Delhi NCR. Environ Monit Assess 187:4146. CrossRefGoogle Scholar
  6. Chaudhari AU, Tapase SR, Markad VL, Kodam KM (2013) Simultaneous decolorization of reactive Orange M2R dye and reduction of chromate by Lysinibacillus sp. KMK-A. J Hazard Mater 262:580–588. CrossRefGoogle Scholar
  7. Das SK, Mukherjee M, Guha AK (2008) Interaction of chromium with resistant strain Aspergillus versicolor: investigation with atomic force microscopy and other physical studies. Langmuir 24:8643–8650. CrossRefGoogle Scholar
  8. Dey P, Gola D, Mishra A et al (2016) Comparative performance evaluation of multi-metal resistant fungal strains for simultaneous removal of multiple hazardous metals. J Hazard Mater.
  9. Ge W, Zamri D, Mineyama H, Valix M (2011) Bioaccumulation of heavy metals on adapted Aspergillus foetidus. Adsorption 17:901–910. CrossRefGoogle Scholar
  10. Geva P, Kahta R, Nakonechny F et al (2016) Increased copper bioremediation ability of new transgenic and adapted Saccharomyces cerevisiae strains. Environ Sci Pollut Res 23:19613–19625. CrossRefGoogle Scholar
  11. Gola D, Namburath M, Kumar R (2015) Decolourization of the Azo dye (direct brilliant blue) by the isolated bacterial strain. J Basic Appl Eng Res 2:1462–1465Google Scholar
  12. Gola D, Dey P, Bhattacharya A et al (2016a) Multiple heavy metal removal using an entomopathogenic fungi Beauveria bassiana. Bioresour Technol 218:388–396. CrossRefGoogle Scholar
  13. Gola D, Malik A, Shaikh ZA, Sreekrishnan TR (2016b) Impact of heavy metal containing wastewater on agricultural soil and produce: relevance of biological treatment. Environ Process 3:1063–1080. CrossRefGoogle Scholar
  14. Gola D, Chauhan N, Malik A, Shaikh ZA, Sreekrishnan TR (2017) Bioremediation approach for handling multiple metal contamination. Handbook of metal-microbe interactions and bioremediation (pp 471-491). CRC Press, Boca Raton.
  15. Gupta SK, Chabukdhara M, Kumar P et al (2014) Evaluation of ecological risk of metal contamination in river Gomti, India: a biomonitoring approach. Ecotoxicol Environ Saf 110:49–55. CrossRefGoogle Scholar
  16. Iram S, Shabbir R, Zafar H, Javaid M (2015) Biosorption and bioaccumulation of copper and lead by heavy metal-resistant fungal isolates. Arab J Sci Eng 40:1867–1873. CrossRefGoogle Scholar
  17. Jing W, Shiying HE, Lina XU, Ning GU (2007) Transmission electron microscopy and atomic force microscopy characterization of nickel deposition on bacterial cells. Chin Sci Bull 52:2919–2924. CrossRefGoogle Scholar
  18. Kameo S, Iwahashi H, Kojima Y, Satoh H (2000) Induction of metallothioneins in the heavy metal resistant fungus Beauveria bassiana exposed to copper or cadmium. Analusis 28:382–385. CrossRefGoogle Scholar
  19. Kaushik P, Malik A (2010) Effect of nutritional conditions on dye removal from textile effluent by Aspergillus lentulus. World J Microbiol Biotechnol 26:1957–1964. CrossRefGoogle Scholar
  20. Kaushik P, Malik A (2013) Comparative performance evaluation of Aspergillus lentulus for dye removal through bioaccumulation and biosorption. Environ Sci Pollut Res 20:2882–2892. CrossRefGoogle Scholar
  21. Kaushik P, Mishra A, Malik A, Sharma S (2015) Production and shelf life evaluation of storable myco-granules for multiple environmental applications. Int Biodeterior Biodegrad 100:70–78. CrossRefGoogle Scholar
  22. Kayama F, Fatmi Z, Ikegami A et al (2016) Exposure assessment of lead from food and airborne dusts and biomonitoring in pregnant mothers, their fetus and siblings in Karachi, Pakistan and Shimotsuke, Japan. Rev Environ Health 31:33–35.
  23. Khani R, Moudi M, Khojeh V (2017) Contamination level, distribution and health risk assessment of heavy and toxic metallic and metalloid elements in a cultivated mushroom Pleurotus florida (Mont.) singer. Environ Sci Pollut Res 24:4699–4708.
  24. Khodabakhsh F, Nazeri S, Amoozegar MA, Khodakaramian G (2011) Isolation of a moderately halophilic bacterium resistant to some toxic metals from Aran & Bidgol Salt Lake and its phylogenetic characterization by 16S rDNA gene. Feyz J Kashan Univ Med Sci 15:53–60Google Scholar
  25. Liu W, Liu C, Liu L et al (2017) Simultaneous decolorization of sulfonated azo dyes and reduction of hexavalent chromium under high salt condition by a newly isolated salt-tolerant strain Bacillus circulans BWL1061. Ecotoxicol Environ Saf 141:9–16. CrossRefGoogle Scholar
  26. Lokhande RS, Singare UP, Pimple DS (2011) Quantification study of toxic heavy metal pollutants in sediment samples collected from Kasardi River flowing along the Taloja industrial area of Mumbai, India. New York Sci J 4:66–71Google Scholar
  27. Maqbool Z, Hussain S, Ahmad T et al (2016) Use of RSM modeling for optimizing decolorization of simulated textile wastewater by Pseudomonas aeruginosa strain ZM130 capable of simultaneous removal of reactive dyes and hexavalent chromium. Environ Sci Pollut Res 23:11224–11239. CrossRefGoogle Scholar
  28. Martinello M, Dainese N, Manzinello C et al (2016) Retrospective evaluation of lead contamination in honey from 2005 to present in northeastern Italy and future perspectives in the light of updated legislation. Food Addit Contam, Part B 9:198–202. CrossRefGoogle Scholar
  29. Mathur M, Vijayalakshmi KS, Gola D, Singh K (2015) Decolourization of textile dyes by Aspergillus lentulus. J Basic Appl Eng Res 2:1469–1473Google Scholar
  30. Miller G (1959) Determination of reducing sugar by DNS method. Anal chem 31:426–428Google Scholar
  31. Mishra A (2013) Development of biological system employing microbial consortium for pollutant removal from mixed waste stream. PhD Thesis, Indian Institute of Technology Delhi, pp 1–254Google Scholar
  32. Mishra A, Malik A (2012) Simultaneous bioaccumulation of multiple metals from electroplating effluent using Aspergillus lentulus. Water Res 46:4991–4998. CrossRefGoogle Scholar
  33. Mishra A, Malik A (2014a) Novel fungal consortium for bioremediation of metals and dyes from mixed waste stream. Bioresour Technol 171:217–226. CrossRefGoogle Scholar
  34. Mishra A, Malik A (2014b) Novel fungal consortium for bioremediation of metals and dyes from mixed waste stream. Bioresour Technol 171:217–226. CrossRefGoogle Scholar
  35. Mishra A, Malik A (2014c) Metal and dye removal using fungal consortium from mixed waste stream: optimization and validation. Ecol Eng 69:226–231. CrossRefGoogle Scholar
  36. Mishra S, Singh SN, Pande V (2014) Bacteria induced degradation of fluoranthene in minimal salt medium mediated by catabolic enzymes in vitro condition. Bioresour Technol 164:299–308. CrossRefGoogle Scholar
  37. Moore BA, Duncan JR, Burgess JE (2008) Fungal bioaccumulation of copper, nickel, gold and platinum. Miner Eng 21:55–60. CrossRefGoogle Scholar
  38. Muñoz AJ, Espínola F, Ruiz E (2016) Removal of Pb(II) in a packed-bed column by a Klebsiella sp. 3S1 biofilm supported on porous ceramic Raschig rings. J Ind Eng Chem 40:118–127. CrossRefGoogle Scholar
  39. Purchase D, Scholes LNL, Revitt DM, Shutes RBE (2009) Effects of temperature on metal tolerance and the accumulation of Zn and Pb by metal-tolerant fungi isolated from urban runoff treatment wetlands. J Appl Microbiol 106:1163–1174. CrossRefGoogle Scholar
  40. Rehner SA (2005) Phylogenetics of the insect pathogenic genus Beauveria. Oxford Univ Press, New York, pp 3–27Google Scholar
  41. Roba C, Roşu C, Piştea I et al (2016) Heavy metal content in vegetables and fruits cultivated in Baia Mare mining area (Romania) and health risk assessment. Environ Sci Pollut Res Int 23:6062–6073. CrossRefGoogle Scholar
  42. Ruadrew S, Craft J, Aidoo K (2013) Occurrence of toxigenic Aspergillus spp. and aflatoxins in selected food commodities of Asian origin sourced in the West of Scotland. Food Chem Toxicol 55:653–658Google Scholar
  43. Seyis I, Subasioglu T (2008) Comparison of live and dead biomass of fungi on decolorization of methyl orange. African J Biotechnol 7:2212–2216Google Scholar
  44. Shah M (2014) Eco-friendly treatment of acid red by an application of Pseudomonas spp. Int J Environ Bioremediation Biodegrad 2:62–68Google Scholar
  45. Sheng J, Qiu W, Xu B et al (2016) Monitoring of heavy metal levels in the major rivers and in residents’ blood in Zhenjiang City, China, and assessment of heavy metal elimination via urine and sweat in humans. Environ Sci Pollut Res:1–12.
  46. Širić I, Humar M, Kasap A et al (2016) Heavy metal bioaccumulation by wild edible saprophytic and ectomycorrhizal mushrooms. Environ Sci Pollut Res 23:18239–18252. CrossRefGoogle Scholar
  47. Srivastava S, Thakur IS (2006) Biosorption potency of Aspergillus niger for removal of chromium (VI). Curr Microbiol 53:232–237. CrossRefGoogle Scholar
  48. Tyagi AK, Malik A (2010) In situ SEM, TEM and AFM studies of the antimicrobial activity of lemon grass oil in liquid and vapour phase against Candida albicans. Micron 41:797–805. CrossRefGoogle Scholar
  49. Wang T, Sun H (2013) Biosorption of heavy metals from aqueous solution by UV-mutant Bacillus subtilis. Environ Sci Pollut Res Int 20:7450–7463. CrossRefGoogle Scholar
  50. Yadav AK, Kumar N, Sreekrishnan TR et al (2010) Removal of chromium and nickel from aqueous solution in constructed wetland: mass balance, adsorption–desorption and FTIR study. Chem Eng J 160:122–128. CrossRefGoogle Scholar
  51. Yilmazer P, Saracoglu N (2009) Bioaccumulation and biosorption of copper(II) and chromium(III) from aqueous solutions by Pichia stipitis yeast. J Chem Technol Biotechnol 84:604–610. CrossRefGoogle Scholar
  52. Zhou Q (2001) Chemical pollution and transport of organic dyes in water-soil-crop systems of the Chinese coast. Bull Environ Contam Toxicol 66:784–793. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Deepak Gola
    • 1
  • Anushree Malik
    • 1
    Email author
  • Maneesh Namburath
    • 1
  • Shaikh Ziauddin Ahammad
    • 2
  1. 1.Applied Microbiology LaboratoryCentre for Rural Development and TechnologyNew DelhiIndia
  2. 2.Department of Biochemical Engineering & BiotechnologyIndian Institute of TechnologyDelhiIndia

Personalised recommendations