Indian Journal of Microbiology

, Volume 58, Issue 2, pp 182–192 | Cite as

Potential of Marine-Derived Fungi to Remove Hexavalent Chromium Pollutant from Culture Broth

  • Nikita P. Lotlikar
  • Samir R. Damare
  • Ram Murti Meena
  • P. Linsy
  • Brenda Mascarenhas
Original Research Article
  • 55 Downloads

Abstract

Chromium (Cr) released from industrial units such as tanneries, textile and electroplating industries is detrimental to the surrounding ecosystems and human health. The focus of the present study was to check the Cr(VI) removal efficiency by marine-derived fungi from liquid broth. Amongst the three Cr(VI) tolerant isolates, #NIOSN-SK56-S19 (Aspergillus sydowii) showed Cr-removal efficiency of 0.01 mg Cr mg−1 biomass resulting in 26% abatement of total Cr with just 2.8 mg of biomass produced during the growth in 300 ppm Cr(VI). Scanning Electron Microscopy revealed aggregation of mycelial biomass with exopolysaccharide, while Electron Dispersive Spectroscopy showed the presence of Cr2O3 inside the biomass indicating presence of active Cr(VI) removal mechanisms. This was further supported when the Cr(VI) removal was monitored using DPC (1,5-diphenylcarbazide) method. The results of this study point to the potential of marine-derived fungal isolates for Cr(VI) removal.

Keywords

Biosorption Halotolerant Heavy metal Hexavalent chromium Marine-derived fungi 

Notes

Acknowledgements

The first author is thankful to Council of Scientific and Industrial Research (CSIR) for the fellowship (Ref No.: 18-12/2011(ii)EU-V). All the authors are thankful to Head, BOD and Director, CSIR-NIO for the facilities. The studies were funded through the Project PSC0206. The authors are thankful to Mr. Areef Sardar for carrying out SEM and EDS analysis. This work is part of the doctoral thesis to be submitted to Goa University in Department of Microbiology. The manuscript is NIO contribution No. 6186.

Compliance with Ethical Standards

Conflict of interest

The authors declare no financial or commercial conflict of interest.

Supplementary material

12088_2018_719_MOESM1_ESM.doc (712 kb)
Supplementary material 1 (DOC 711 kb)

References

  1. 1.
    Beveridge TJ, Hughes MN, Leung KT, Poole RK, Savvaidis I, Silver S, Trevors JT (1997) Metal-microbe interactions: contemporary approaches. Adv Microb Physiol 38:177–243CrossRefPubMedGoogle Scholar
  2. 2.
    Ahmad I, Ansari MI, Aqil F (2006) Biosorption of Ni, Cr and Cd by metal tolerant Aspergillus niger and Penicillium sp. using single and multi-metal solution. Indian J Exp Biol 44:73–76PubMedGoogle Scholar
  3. 3.
    Hasan HAH (2007) Role of rock phosphate in alleviation of heavy metals stress on Fusarium oxysporum. Plant Soil Environ 53:1–6CrossRefGoogle Scholar
  4. 4.
    Joshi PK, Swarup A, Maheshwari S, Kumar R, Singh N (2011) Bioremediation of heavy metals in liquid media through fungi isolated from contaminated sources. Indian J Microbiol 51:482–487.  https://doi.org/10.1007/s12088-011-0110-9 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bishnoi NR, Garima (2005) Fungus- an alternative for bioremediation of heavy metal containing wastewater: a review. J Sci Ind Res India 64:93–100Google Scholar
  6. 6.
    Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Biol 53:1–11.  https://doi.org/10.1093/jexbot/53.366.1 Google Scholar
  7. 7.
    Bellion M, Courbot M, Jacob C, Blaudez Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi—a minireview. FEMS Microbiol Lett 254:173–181.  https://doi.org/10.1111/j.1574-6968.2005.00044.x CrossRefPubMedGoogle Scholar
  8. 8.
    Borut P, Istvan P, Peter R, Pesti M (2010) Interference of chromium with biological systems in yeasts and fungi: a review. J Basic Microbiol 50:21–36.  https://doi.org/10.1002/jobm.200900170 CrossRefGoogle Scholar
  9. 9.
    Nazareth S, Gaitonde S, Marbaniang T (2012) Metal resistance of halotolerant fungi from mangroves and salterns of Goa, India. Kavaka 40:15–21Google Scholar
  10. 10.
    Gunde-Cimerman N, Ramos J, Plemenitas A (2009) Halotolerant and halophilic fungi: a review. Mycol Res 113:1231–1241.  https://doi.org/10.1016/j.mycres.2009.09.002 CrossRefPubMedGoogle Scholar
  11. 11.
    Hamedi J, Fatemeh M, Hamed KSP (2015) Biotechnological exploitation of actinobacterial members. In: Maheshwari DK, Saraf M (eds) Halophiles—biodiversity and sustainable exploitation. Springer, Switzerland.  https://doi.org/10.1007/978-3-319-14595-2 Google Scholar
  12. 12.
    Rulcker CK, Allard B, Schnurer J (1993) Interactions between a soil fungus, Trichoderma harzianum, and IIb metals-adsorption of mycelium and production of complexing metabolites. Biometals 6:223–230.  https://doi.org/10.1007/BF00187759 Google Scholar
  13. 13.
    Parvathi K, Nareshkumar R, Nagendran R (2007) Biosorption of manganese by Aspergillus niger and Saccharomyces cerevisiae. World J Microbiol Biot 23:671–676.  https://doi.org/10.1007/s11274-006-9281-7 CrossRefGoogle Scholar
  14. 14.
    Subbaiah MV, Yun YS (2013) Biosorption of nickel (II) from aqueous solution by the fungal mat of Trametes versicolor (Rainbow) biomass: equilibrium, kinetics, and thermodynamic studies. Biotechnol Bioprocess Eng 18:280–288.  https://doi.org/10.1007/s12257-012-0401-y CrossRefGoogle Scholar
  15. 15.
    Akhtar S, Hassan MM, Ahmad R, Suthor V, Yasin M (2013) Metal tolerance potential of filamentous fungi isolated from soils irrigated with untreated municipal effluent. Soil Environ 32:55–62Google Scholar
  16. 16.
    White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA et al (eds) PCR protocols: a guide to methods and applications. Academic Press, New York.  https://doi.org/10.1016/b978-0-12-372180-8.50042-1 Google Scholar
  17. 17.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410.  https://doi.org/10.1016/S0022-2836(05)80360-2 CrossRefPubMedGoogle Scholar
  18. 18.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739.  https://doi.org/10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Hseu ZY (2004) Evaluating heavy metal contents in nine composts using four digestion methods. Biores Technol 95:53–59.  https://doi.org/10.1016/j.biortech.2004.02.008 CrossRefGoogle Scholar
  20. 20.
    Pfalaum R, Howick L (1956) The chromium-diphenylcarbazide reaction. J Am Chem Soc 78:4862–4866.  https://doi.org/10.1021/ja01600a014 CrossRefGoogle Scholar
  21. 21.
    Damare VS (2015) Diversity of thraustochytrid protists isolated from brown alga, Sargassum cinereum using 18S rDNA sequencing and their morphological response to heavy metals. J Mar Biol Assoc UK 95:265–276.  https://doi.org/10.1017/S0025315414001696 CrossRefGoogle Scholar
  22. 22.
    Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation and rehabilitation of mangrove ecosystems: an overview. Biol Fertil Soils 33:265–278.  https://doi.org/10.1007/s003740000319 CrossRefGoogle Scholar
  23. 23.
    Raghukumar S, Raghukumar C, Manohar CS (2014) Fungi living in diverse extreme habitats of the marine environment. Kavaka 42:145–153Google Scholar
  24. 24.
    Chakraborty P, Ramteke D, Chakraborty S (2015) Geochemical partitioning of Cu and Ni in mangrove sediments: relationships with their bioavailability. Mar Pollut Bull 93:194–201.  https://doi.org/10.1016/j.marpolbul.2015.01.016 CrossRefPubMedGoogle Scholar
  25. 25.
    Nayak SS, Gonsalves V, Nazareth SW (2012) Isolation and salt tolerance of halophilic fungi from mangroves and solar salterns in Goa-India. Indian J Geomar Sci 41:164–172Google Scholar
  26. 26.
    Babich H, Gamba-Vitalo C, Stotsky G (1982) Comparative toxicity of nickel to mycelia proliferation and spore formation of selected fungi. Arch Environ Contam Toxicol 11:465–468CrossRefGoogle Scholar
  27. 27.
    Al-Abboud MA, Alawlaqi MM (2011) Biouptake of copper and their impact on fungal fatty acids. Aust J Basic Appl Sci 5:283–290Google Scholar
  28. 28.
    Zapotoczny S, Jurkiewicz A, Tylko G, Anielska T, Turnau K (2007) Accumulation of copper by Acremonium pinkertoniae, a fungus isolated from industrial wastes. Microbiol Res 162:219–228.  https://doi.org/10.1016/j.micres.2006.03.008 CrossRefPubMedGoogle Scholar
  29. 29.
    Valix M, Loon LO (2003) Adaptive tolerance behaviour of fungi in heavy metals. Miner Eng 16:193–198.  https://doi.org/10.1016/S0892-6875(03)00004-9 CrossRefGoogle Scholar
  30. 30.
    Rajapaksha RMCP, Tobor-Kaplon MA, Baath E (2004) Metal toxicity affects fungal and bacterial activities in soil differently. Appl Environ Microbiol 70:2966–2973.  https://doi.org/10.1128/AEM.70.5.2966-2973.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Akthar MN, Sastry KS, Mohan PM (1996) Mechanism of metal ion biosorption by fungal biomass. Biometals 9:21–28.  https://doi.org/10.1007/BF00188086 CrossRefGoogle Scholar
  32. 32.
    Faryal R, Lodhi A, Hameed A (2006) Isolation, Characterization and biosorption of Zinc by indigenous fungal strains Aspergillus fumigatus RH05 and Aspergillus flavus RH07. Pak J Bot 38:817–832Google Scholar
  33. 33.
    Abbas SH, Ismail IM, Mostafa TM, Sulaymon AH (2014) Biosorption of heavy metals : a review. J Chem Sci Technol 3:74–102Google Scholar
  34. 34.
    Merrie JS, Sheela R, Saswathi N, Prakasham RS, Ramakrishna SV (1998) Biosorption of chromium VI using Rhizopus arrhizus. Indian J Exp Biol 36:1052–1055Google Scholar
  35. 35.
    Jakubiak M, Giska I, Asztemborska M, Bystrzejewska-Piotrowska G (2014) Bioaccumulation and biosorption of inorganic nanoparticles: factors affecting the efficiency of nanoparticle mycoextraction by liquid- grown mycelia of Pleurotus eryngii and Trametes versicolor. Mycol Prog 13:525–532.  https://doi.org/10.1007/s11557-013-0933-3 CrossRefGoogle Scholar
  36. 36.
    Coogeevaram S, Dhanarani S, Park J, Dexilin M, Thamaraiselvi K (2007) Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. J Hazard Mater 146:270–277.  https://doi.org/10.1016/j.jhazmat.2006.12.017 CrossRefGoogle Scholar
  37. 37.
    Sen M (2012) A comparative study on biosorption of Cr(VI) by Fusarium solani under different growth conditions. Open J Appl Sci 2:146–152.  https://doi.org/10.4236/ojapps.2012.23021 CrossRefGoogle Scholar
  38. 38.
    Annamalai K, Nair AM, Chinnaraju S, Kuppusamy S (2014) Chromium (III) nanoparticles synthesis using the biosorption and bioreduction with Bacillus subtilis: effect of pH and temperature. Int J ChemTech Res 6:1910–1912Google Scholar
  39. 39.
    Annamalai K, Nair AM, Chinnaraju S, Kuppusamy S (2014) Removal of chromium from contaminated effluent and simultaneously green nanoparticle synthesis using Bacillus subtilis. Malaya J Biosci 1:13–18Google Scholar
  40. 40.
    Chandra S, Kumar A (2013) Spectral, thermal and morphological studies of chromium nanoparticles. Spectrochim Acta A 102:250–255.  https://doi.org/10.1016/j.saa.2012.10.003 CrossRefGoogle Scholar
  41. 41.
    Jaswal VS, Arora AK, Kinger M, Gupta VD, Singh J (2014) Synthesis and characterization of chromium oxide nanoparticles. Orient J Chem 30:559–566.  https://doi.org/10.13005/ojc/300220 CrossRefGoogle Scholar
  42. 42.
    Mohite PT, Kumar AR, Zinjarde SS (2016) Biotransformation of hexavalent chromium into extracellular chromium (III) oxide nanoparticles using Schwanniomyces occidentalis. Biotechnol Lett 38:441–446.  https://doi.org/10.1007/s10529-015-2009-8 CrossRefPubMedGoogle Scholar
  43. 43.
    Focardi S, Pepi M, Focardi SE (2013) Microbial reduction of hexavalent chromium as a mechanism of detoxification and possible bioremediation applications. In: Chamy R, Rosenkranz F (eds) Biodegradation-life of science. InTech, Rijeka, pp 321–347.  https://doi.org/10.5772/56365 Google Scholar
  44. 44.
    Baldrian P, Gabriel J (2003) Adsorption of heavy metal on microbial biomass: Use of biosorption for removal metals from metal solutions. In: Sasek V et al (eds) The utilization of bioremediation to reduce soil contamination: problems and solutions, vol 19. Springer, DordrechtGoogle Scholar
  45. 45.
    White C, Wilkinson SC, Gadd GM (1995) The role of microorganisms in biosorption of toxic metals and radio nuclides. Int Biodeterior Biodegrad.  https://doi.org/10.1016/0964-8305(95)00036-5 Google Scholar
  46. 46.
    Liu Y, Lam MC, Fang HHP (2001) Adsorption of heavy metals by EPS of activated sludge. Water Sci Technol 43:59–66PubMedGoogle Scholar
  47. 47.
    Faisal M, Hasnain S (2004) Comparative study of Cr(VI) uptake and reduction in industrial effluent by Ochrobactrum intermedium and Brevibacterium sp. Biotechnol Lett 26:1623–1628CrossRefPubMedGoogle Scholar
  48. 48.
    Wang YT, Shen H (1995) Bacterial reduction of hexavalent chromium. J Ind Microbiol 14:159–163.  https://doi.org/10.1007/BF01569898 CrossRefPubMedGoogle Scholar
  49. 49.
    Prakasham RS, Merrie JS, Sheela R, Saswathi N, Ramakrishna SV (1999) Biosorption of chromium VI by free and immobilized Rhizopus arrhizus. Environ Pollut 104:421–427.  https://doi.org/10.1016/S0269-7491(98)00174-2 CrossRefGoogle Scholar
  50. 50.
    Sudha BR, Abraham TE (2001) Biosorption of Cr(VI) from aqueous solution by Rhizopus nigricans. Bioresour Technol 79:73–81.  https://doi.org/10.1016/S0960-8524(00)00107-3 CrossRefGoogle Scholar
  51. 51.
    Kumar R, Singh P, Dhir B, Sharma AK, Mehta D (2014) Potential of some fungal and bacterial species in bioremediation of heavy metals. J Nucl Phys 1:213–223.  https://doi.org/10.15415/jnp.2014.12017 Google Scholar

Copyright information

© Association of Microbiologists of India 2018

Authors and Affiliations

  1. 1.Biological Oceanography DivisionCSIR-National Institute of OceanographyDona PaulaIndia
  2. 2.Geological Oceanography DivisionCSIR-National Institute of OceanographyDona PaulaIndia

Personalised recommendations