Main Article Content

Abstract

The main polluting source of heavy metal contamination of water is the leather tanning industry, which uses chrome powder and discharges it into the nearby ecosystem. In this investigation, chromium-resistant bacterial strains were isolated and characterized from tannery effluent. Based on morphological and biochemical characterization, the predominant sporulating Bacillus sp. was isolated and identified as Bacillus subtilis based on 16S rRNA gene sequencing. Chromium degradation by the bacterial strain was evaluated using the flask culture method at three different concentrations (300, 600, and 900 µg/ml) of Cr (VI), and the reduction potential of the isolated bacterium was analyzed by Atomic Absorption Spectrophotometry. A maximum reduction of approximately 78% was found at 24 hrs of incubation at pH 7 and at a constant temperature of 30°C. More than 50% of the Cr(VI) was decreased in 24 hours when the Cr(VI) concentration varied from 300 to 900 g/ml. FTIR analysis showed the involvement of hydroxyl and amine groups in chromium adsorption. As an outcome, this strain could be a promising bioagent for the environmentally friendly elimination of toxic Cr(VI) from polluted environments.

Keywords

Environmental Pollution Heavy Metal Toxicity Bacillus subtilis Bioremediation Chromium (VI)

Article Details

How to Cite
Reena, & A, J. (2023). Hexavalent chromium bioreduction by chromium-resistant sporulating bacteria isolated from tannery effluent. Environment Conservation Journal, 24(4), 32–44. https://doi.org/10.36953/ECJ.22792588

References

  1. Ahalya, N., Ramachandra, T. V., & Kanamadi, R. D. (2003). Biosorption of heavy metals. Res. J. Chem. Environ, 7(4), 71-79.
  2. Ahamad, F. Bhutiani, R. & Ruhela, M. (2022). Environmental Quality Monitoring Using Environmental Quality Indices (EQI), Geographic Information System (GIS), and Remote Sensing: A Review. GIScience for the Sustainable Management of Water Resources, 331. (Chapter number-18, pp.331-348, ISBN ebook: 9781003284512). DOI: https://doi.org/10.1201/9781003284512-21
  3. Ahmad, S., Mfarrej, M. F. B., El-Esawi, M. A., Waseem, M., Alatawi, A., Nafees, M., ... & Ali, S. (2022). Chromium-resistant Staphylococcus aureus alleviates chromium toxicity by developing synergistic relationships with zinc oxide nanoparticles in wheat. Ecotoxicology and Environmental Safety, 230, 113142. https://doi.org/10.1016/j.ecoenv.2021.113142 DOI: https://doi.org/10.1016/j.ecoenv.2021.113142
  4. Akan, J. C., Moses, E. A., Ogugbuaja, V. O., & Abah, J. (2007). Assessment of tannery industrial effluents from Kano metropolis, Kano State, Nigeria. Journal of Applied Sciences, 7(19), 2788-2793 DOI: https://doi.org/10.3923/jas.2007.2788.2793
  5. Alam, M. Z., & Malik, A. (2008). Chromate resistance, transport and bioreduction by Exiguobacterium sp. ZM‐2 isolated from agricultural soil irrigated with tannery effluent. Journal of basic microbiology, 48(5), 416-420. https://doi.org/10.1002/jobm.200800046 DOI: https://doi.org/10.1002/jobm.200800046
  6. Arahal, D. R., Ludwig, W., Schleifer, K. H., & Ventosa, A. (2002). Phylogeny of the family Halomonadaceae based on 23S and 165 rDNA sequence analyses. International Journal of Systematic and Evolutionary Microbiology, 52(1), 241-249. https://doi.org/10.1099/00207713-52-1-241 DOI: https://doi.org/10.1099/00207713-52-1-241
  7. Bağcıoğlu, M., Fricker, M., Johler, S., & Ehling-Schulz, M. (2019). Detection and identification of Bacillus cereus, Bacillus cytotoxicus, Bacillus thuringiensis, Bacillus mycoides and Bacillus weihenstephanensis via machine learning based FTIR spectroscopy. Frontiers in microbiology, 10, 902. https://doi.org/10.3389/fmicb.2019.00902 DOI: https://doi.org/10.3389/fmicb.2019.00902
  8. Barthwal, J., Smitha, N. A. I. R., & Kakkar, P. (2008). Heavy metal accumulation in medicinal plants collected from environmentally different sites. Biomedical and environmental sciences, 21(4), 319-324. https://doi.org/10.1016/S0895-3988(08)60049-5 DOI: https://doi.org/10.1016/S0895-3988(08)60049-5
  9. Bharagava, R. N., & Mishra, S. (2018). Hexavalent chromium reduction potential of Cellulosimicrobium sp. isolated from common effluent treatment plant of tannery industries. Ecotoxicology and Environmental Safety, 147, 102-109. https://doi.org/10.1016/j.ecoenv.2017.08.040 DOI: https://doi.org/10.1016/j.ecoenv.2017.08.040
  10. Bhardwaj, S., Khanna, D. R., Ruhela, M., Bhutiani, R., Bhardwaj, R., & Ahamad, F. (2020). Assessment of the soil quality of Haridwar Uttarakhand India: A comparative study. Environment Conservation Journal, 21(3), 155-164. DOI: https://doi.org/10.36953/ECJ.2020.21319
  11. Bhutiani, R., & Ahamad, F. (2018). Efficiency assessment of Sand Intermittent Filtration Technology for waste water Treatment. International Journal of advance research in science and engineering (IJARSE), 7(03), 503-512.
  12. Bhutiani, R., Ahamad, F., & Ram, K. (2021). Quality assessment of groundwater at laksar block, haridwar in uttarakhand, India using water quality index: a case study. Journal of Applied and Natural Science, 13(1), 197-203. DOI: https://doi.org/10.31018/jans.v13i1.2435
  13. Bhutiani, R., Ahamad, F., & Ruhela, M. (2021). Effect of composition and depth of filter-bed on the efficiency of Sand-intermittent-filter treating the Industrial wastewater at Haridwar, India. Journal of Applied and Natural Science, 13(1), 88-94. DOI: https://doi.org/10.31018/jans.v13i1.2421
  14. Bhutiani, R., Tiwari, R. C., Chauhan, P., Ahamad, F., Sharma, V. B., Tyagi, I., & Singh, P. (2022). Potential of Cassia fistula pod-based absorbent in remediating water pollutants: An analytical study. In Sustainable Materials for Sensing and Remediation of Noxious Pollutants (pp. 261-272). Elsevier. DOI: https://doi.org/10.1016/B978-0-323-99425-5.00001-3
  15. Bojago, E., Tyagi, I., Ahamad, F., & Chandniha, S. K. (2023). GIS based spatial-temporal distribution of water quality parameters and heavy metals in drinking water: Ecological and health modelling. Physics and Chemistry of the Earth, Parts A/B/C, 103399. DOI: https://doi.org/10.1016/j.pce.2023.103399
  16. Bopp, L. H., Chakrabarty, A. M., & Ehrlich, H. (1983). Chromate resistance plasmid in Pseudomonas fluorescens. Journal of bacteriology, 155(3), 1105-1109. https://doi.org/10.1128/jb.155.3.1105-1109.1983 DOI: https://doi.org/10.1128/jb.155.3.1105-1109.1983
  17. Camargo, F. A. O., Bento, F. M., Okeke, B. C., & Frankenberger, W. T. (2003). Chromate reduction by chromium‐resistant bacteria isolated from soils contaminated with dichromate. Journal of Environmental Quality, 32(4), 1228-1233.
  18. https://doi.org/10.2134/jeq2003.1228 DOI: https://doi.org/10.2134/jeq2003.1228
  19. Cefalu, W. T., & Hu, F. B. (2004). Role of chromium in human health and in diabetes. Diabetes care, 27(11), 2741-2751. https://doi.org/10.2337/diacare.27.11.2741 DOI: https://doi.org/10.2337/diacare.27.11.2741
  20. Cervantes, C., & Campos-García, J. (2007). Reduction and efflux of chromate by bacteria. In Molecular microbiology of heavy metals (pp. 407-419). Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2006_087 DOI: https://doi.org/10.1007/7171_2006_087
  21. Cervantes, C., Campos-García, J., Devars, S., Gutiérrez-Corona, F., Loza-Tavera, H., Torres-Guzmán, J. C., & Moreno-Sánchez, R. (2001). Interactions of chromium with microorganisms and plants. FEMS microbiology reviews, 25(3), 335-347. https://doi.org/10.1111/j.1574-6976.2001.tb00581.x DOI: https://doi.org/10.1111/j.1574-6976.2001.tb00581.x
  22. Chatterjee, S., Ghosh, I., & Mukherjea, K. K. (2011). Uptake and removal of toxic Cr (VI) by Pseudomonas aeruginosa: physico-chemical and biological evaluation. Current Science, 645-652.
  23. Cheung, K. H., & Gu, J. D. (2007). Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. International Biodeterioration & Biodegradation, 59(1), 8-15. https://doi.org/10.1016/j.ibiod.2006.05.002 DOI: https://doi.org/10.1016/j.ibiod.2006.05.002
  24. Chowdhury, M., Mostafa, M. G., Biswas, T. K., & Saha, A. K. (2013). Treatment of leather industrial effluents by filtration and coagulation processes. Water Resources and Industry, 3, 11-22. https://doi.org/10.1016/j.wri.2013.05.002 DOI: https://doi.org/10.1016/j.wri.2013.05.002
  25. Dhal, B., Thatoi, H., Das, N., & Pandey, B. D. (2010). Reduction of hexavalent chromium by Bacillus sp. isolated from chromite mine soils and characterization of reduced product. Journal of Chemical Technology & Biotechnology, 85(11), 1471-1479.
  26. https://doi.org/10.1002/jctb.2451 DOI: https://doi.org/10.1002/jctb.2451
  27. Dong, G., Wang, Y., Gong, L., Wang, M., Wang, H., He, N., & Li, Q. (2013). Formation of soluble Cr (III) end-products and nanoparticles during Cr (VI) reduction by Bacillus cereus strain XMCr-6. Biochemical engineering journal, 70, 166-172.
  28. https://doi.org/10.1016/j.bej.2012.11.002 DOI: https://doi.org/10.1016/j.bej.2012.11.002
  29. Doshi, H., Ray, A., & Kothari, I. L. (2007). Biosorption of cadmium by live and dead Spirulina: IR spectroscopic, kinetics, and SEM studies. Current Microbiology, 54(3), 213-218. https://doi.org/10.1007/s00284-006-0340-y DOI: https://doi.org/10.1007/s00284-006-0340-y
  30. EPA, U. (1998). Toxicological review of hexavalent chromium. Washington, DC.
  31. Fent, K. (2004). Ecotoxicological effects at contaminated sites. Toxicology, 205(3), 223-240. https://doi.org/10.1016/j.tox.2004.06.060 DOI: https://doi.org/10.1016/j.tox.2004.06.060
  32. Ganguli, A., & Tripathi, A. (2002). Bioremediation of toxic chromium from electroplating effluent by chromate-reducing Pseudomonas aeruginosa A2Chr in two bioreactors. Applied Microbiology and Biotechnology, 58(3), 416-420. https://doi.org/10.1007/s00253-001-0871-x DOI: https://doi.org/10.1007/s00253-001-0871-x
  33. Holt, J. G., Krieg, N. R., Sneath, P. H., Staley, J. T., & Williams, S. T. (1994). Bergey's Manual of determinate bacteriology.
  34. Ilias, M., Rafiqullah, I. M., Debnath, B. C., Mannan, K. S. B., & Hoq, M. (2011). Isolation and characterization of chromium (VI)-reducing bacteria from tannery effluents. Indian journal of microbiology, 51(1), 76-81. https://doi.org/10.1007/s12088-011-0095-4 DOI: https://doi.org/10.1007/s12088-011-0095-4
  35. James, B. R., Petura, J. C., Vitale, R. J., & Mussoline, G. R. (1997). Oxidation‐reduction chemistry of chromium: Relevance to the regulation and remediation of chromate‐contaminated soils. Soil and Sediment Contamination, 6(6), 569-580. https://doi.org/10.1080/15320389709383590 DOI: https://doi.org/10.1080/15320389709383590
  36. Jeyasingh, J., & Philip, L. (2005). Bioremediation of chromium contaminated soil: optimization of operating parameters under laboratory conditions. Journal of Hazardous Materials, 118(1-3), 113-120. https://doi.org/10.1016/j.jhazmat.2004.10.003 DOI: https://doi.org/10.1016/j.jhazmat.2004.10.003
  37. Katsayal, B. S., Sallau, A. B., & Muhammad, A. (2022). Kinetics and thermodynamics of Cr (VI) reduction by Tamarindus indica methanol leaves extract under optimized reaction conditions. Beni-Suef University Journal of Basic and Applied Sciences, 11(1), 1-10. https://doi.org/10.1186/s43088-022-00233-z DOI: https://doi.org/10.1186/s43088-022-00233-z
  38. Kavitha, P. R., & Ganapathy, G. P. (2015). Tannery process and its environmental impacts a case study: Vellore District, Tamil Nadu, India. J Chem Pharm Sci, 8, 759-764.
  39. Kobya, M., Demirbas, E., Senturk, E., & Ince, M. (2005). Adsorption of heavy metal ions from aqueous solutions by activated carbon prepared from apricot stone. Bioresource technology, 96(13), 1518-1521. https://doi.org/10.1016/j.biortech.2004.12.005 DOI: https://doi.org/10.1016/j.biortech.2004.12.005
  40. Lace, A., Ryan, D., Bowkett, M., & Cleary, J. (2019). Chromium monitoring in water by colorimetry using optimized 1,5-diphenylcarbazide method. International journal of environmental research and public health, 16(10), 1803. https://doi.org/10.3390/ijerph16101803 DOI: https://doi.org/10.3390/ijerph16101803
  41. Li, M. H., Gao, X. Y., Li, C., Yang, C. L., Fu, C. A., Liu, J., & Pang, X. (2020). Isolation and identification of chromium reducing Bacillus Cereus species from chromium-contaminated soil for the biological detoxification of chromium. International Journal of Environmental Research and Public Health, 17(6), 2118. https://doi.org/10.3390/ijerph17062118
  42. Li, M. H., Gao, X. Y., Li, C., Yang, C. L., Fu, C. A., Liu, J., ... & Pang, X. (2020). Isolation and identification of chromium reducing Bacillus Cereus species from chromium-contaminated soil for the biological detoxification of chromium. International Journal of Environmental Research and Public Health, 17(6), 2118. https://doi.org/10.3390/ijerph17062118 DOI: https://doi.org/10.3390/ijerph17062118
  43. Liu, J., Xue, J., Wei, X., Su, H., & Xu, R. (2020). Optimization of Cr6+ removal by Bacillus subtilis strain SZMC 6179J from chromium-containing soil. Indian journal of microbiology, 60(4), 430-435. https://doi.org/10.1007/s12088-020-00886-3 DOI: https://doi.org/10.1007/s12088-020-00886-3
  44. Mala, J. G. S., Sujatha, D., & Rose, C. (2015). Inducible chromate reductase exhibiting extracellular activity in Bacillus methylotrophicus for chromium bioremediation. Microbiological research, 170, 235-241. https://doi.org/10.1016/j.micres.2014.06.001 DOI: https://doi.org/10.1016/j.micres.2014.06.001
  45. Mishra, R. R., Dhal, B., Dutta, S. K., Dangar, T. K., Das, N. N., & Thatoi, H. N. (2012). Optimization and characterization of chromium (VI) reduction in saline condition by moderately halophilic Vigribacillus sp. isolated from mangrove soil of Bhitarkanika, India. Journal of hazardous materials, 227, 219-226. https://doi.org/10.1016/j.jhazmat.2012.05.063 DOI: https://doi.org/10.1016/j.jhazmat.2012.05.063
  46. Muhammad A, Rakhshan K, Ikhtiar K, Asma S. (2015). Effect of Heavy Metals from Tannery Effluent on the Soil and Groundwater using Multivariate Analysis in District Sheikhupura, Pakistan. Res. J Chem. Environ, 19(1), pp.48-55.
  47. Mungasavalli, D. P., Viraraghavan, T., & Jin, Y. C. (2007). Biosorption of chromium from aqueous solutions by pretreated Aspergillus niger: batch and column studies. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 301(1-3), 214-223. https://doi.org/10.1016/j.colsurfa.2006.12.060 DOI: https://doi.org/10.1016/j.colsurfa.2006.12.060
  48. Murugavelh, S., & Mohanty, K. (2013). Isolation, identification and characterization of Cr (VI) reducing Bacillus cereus from chromium contaminated soil. Chemical Engineering Journal, 230, 1-9. https://doi.org/10.1016/j.cej.2013.06.049 DOI: https://doi.org/10.1016/j.cej.2013.06.049
  49. Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: a review. Environmental chemistry letters, 8(3), 199-216. https://doi.org/10.1007/s10311-010-0297-8 DOI: https://doi.org/10.1007/s10311-010-0297-8
  50. Nandy, T., Kaul, S. N., Shastry, S., Manivel, U., & Deshpande, C. V. (1999). Wastewater management in cluster of tanneries in Tamil Nadu through implementation of common effluent treatment plants: NISCAIR-CSIR, India
  51. Pham, X. N., Nguyen, T. P., Pham, T. N., Tran, T. T. N., & Tran, T. V. T. (2016). Synthesis and characterization of chitosan-coated magnetite nanoparticles and their application in curcumin drug delivery. Advances in Natural Sciences: Nanoscience and Nanotechnology, 7(4), 045010. DOI 10.1088/2043-6262/7/4/045010 DOI: https://doi.org/10.1088/2043-6262/7/4/045010
  52. Piñón‐Castillo, H. A., Brito, E. M. S., Goñi‐Urriza, M., Guyoneaud, R., Duran, R., Nevarez‐Moorillon, G. V., ... & Reyna‐López, G. E. (2010). Hexavalent chromium reduction by bacterial consortia and pure strains from an alkaline industrial effluent. Journal of applied microbiology, 109(6), 2173-2182. https://doi.org/10.1111/j.1365-2672.2010.04849.x DOI: https://doi.org/10.1111/j.1365-2672.2010.04849.x
  53. Polti, M. A., García, R. O., Amoroso, M. J., & Abate, C. M. (2009). Bioremediation of chromium (VI) contaminated soil by Streptomyces sp. MC1. Journal of Basic Microbiology, 49(3), 285-292. https://doi.org/10.1002/jobm.200800239 DOI: https://doi.org/10.1002/jobm.200800239
  54. Rahman, Z., & Singh, V. P. (2019). The relative impact of toxic heavy metals (THMs)(arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: an overview. Environmental monitoring and assessment, 191(7), 1-21.
  55. https://doi.org/10.1007/s10661-019-7528-7 DOI: https://doi.org/10.1007/s10661-019-7528-7
  56. Ray, S., & Ray, M. K. (2009). Bioremediation of heavy metal toxicity-with special reference to chromium. Al Ameen J Med Sci, 2(2), 57-63.
  57. Rolfe, M. D., Rice, C. J., Lucchini, S., Pin, C., Thompson, A., Cameron, A. D., ... & Hinton, J. C. (2012). Lag phase is a distinct growth phase that prepares bacteria for exponential growth and involves transient metal accumulation. Journal of bacteriology, 194(3), 686-701.
  58. https://doi.org/10.1128/JB.06112-11 DOI: https://doi.org/10.1128/JB.06112-11
  59. Romanenko, V. I., & Koren'Kov, V. N. (1977). Pure culture of bacteria using chromates and bichromates as hydrogen acceptors during development under anaerobic conditions. Mikrobiologiia, 46(3), 414-417.
  60. Ruhela, M., Bhardwaj, S., Garg, V., & Ahamad, F. (2022). Assessment of soil quality at selected sites around Karwi town, Chitrakoot (Uttar Pradesh), India. Archives of Agriculture and Environmental Science, 7(3), 379-385. DOI: https://doi.org/10.26832/24566632.2022.0703011
  61. Ruhela, M., Bhutiani, R., Ahamad, F., & Khanna, D. R. (2019). Impact of Hindon River Water on Selected Riparian Flora (Azadirachta Indica and Acacia Nilotica) with special Reference to Heavy Metals. Pollution, 5(4), 749-760.
  62. Sambrook J, Fritsch EF, Maniatis T. (1989) Molecular cloning: a laboratory manual. Cold spring harbor laboratory press
  63. Sathishkumar, K., Murugan, K., Benelli, G., Higuchi, A., & Rajasekar, A. (2017). Bioreduction of hexavalent chromium by Pseudomonas stutzeri L1 and Acinetobacter baumannii L2. Annals of Microbiology, 67(1), 91-98. https://doi.org/10.1007/s13213-016-1240-4 DOI: https://doi.org/10.1007/s13213-016-1240-4
  64. Selvi, A., Salam, J. A., & Das, N. (2014). Biodegradation of cefdinir by a novel yeast strain, Ustilago sp. SMN03 isolated from pharmaceutical wastewater. World Journal of Microbiology and Biotechnology, 30(11), 2839-2850. https://doi.org/10.1007/s11274-014-1710-4 DOI: https://doi.org/10.1007/s11274-014-1710-4
  65. Seragadam, P., Rai, A., Ghanta, K. C., Srinivas, B., Lahiri, S. K., & Dutta, S. (2021). Bioremediation of hexavalent chromium from wastewater using bacteria-a green technology. Biodegradation, 32(4), 449-466. https://doi.org/10.1007/s10532-021-09947-w DOI: https://doi.org/10.1007/s10532-021-09947-w
  66. Shahadat, M., Rafatullah, M., & Teng, T. T. (2015). Characterization and sorption behavior of natural adsorbent for exclusion of chromium ions from industrial effluents. Desalination and water treatment, 53(5), 1395-1403. https://doi.org/10.1080/19443994.2013.855678 DOI: https://doi.org/10.1080/19443994.2013.855678
  67. Shen, H., & Wang, Y. T. (1993). Characterization of enzymatic reduction of hexavalent chromium by Escherichia coli ATCC 33456. Applied and Environmental Microbiology, 59(11), 3771-3777. https://doi.org/10.1128/aem.59.11.3771-3777.1993 DOI: https://doi.org/10.1128/aem.59.11.3771-3777.1993
  68. Sun, W., Xiao, E., Krumins, V., Häggblom, M. M., Dong, Y., Pu, Z., ... & Li, F. (2018). Rhizosphere microbial response to multiple metal (loid) s in different contaminated arable soils indicates crop-specific metal-microbe interactions. Applied and environmental microbiology, 84(24), e00701-18. https://doi.org/10.1128/AEM.00701-18 DOI: https://doi.org/10.1128/AEM.00701-18
  69. Sundari, N. S. (2017). Characterization of chromium bioremediation by Stenotrophomonas maltophilia SRS 05 isolated from tannery effluent. Int Res J Eng Technol [Internet], 4(2), 403
  70. Thacker, U., Parikh, R., Shouche, Y., & Madamwar, D. (2007). Reduction of chromate by cell-free extract of Brucella sp. isolated from Cr (VI) contaminated sites. Bioresource technology, 98(8), 1541-1547. https://doi.org/10.1016/j.biortech.2006.06.011 DOI: https://doi.org/10.1016/j.biortech.2006.06.011
  71. Trivedy, R. K., & Goel, P. K. (1984). Chemical and biological methods for water pollution studies. Environmental publications.
  72. Verma, T., Ramteke, P. W., & Garg, S. K. (2008). Quality assessment of treated tannery wastewater with special emphasis on pathogenic E. coli detection through serotyping. Environmental monitoring and assessment, 145(1), 243-249.
  73. https://doi.org/10.1007/s10661-007-0033-4 DOI: https://doi.org/10.1007/s10661-007-0033-4
  74. Wang, P. C., Mori, T., Komori, K., Sasatsu, M., Toda, K., & Ohtake, H. (1989). Isolation and characterization of an Enterobacter cloacae strain that reduces hexavalent chromium under anaerobic conditions. Applied and Environmental Microbiology, 55(7), 1665-1669. https://doi.org/10.1128/aem.55.7.1665-1669.1989 DOI: https://doi.org/10.1128/aem.55.7.1665-1669.1989
  75. Wang, Y. T., & Xiao, C. (1995). Factors affecting hexavalent chromium reduction in pure cultures of bacteria. Water Research, 29(11), 2467-2474. https://doi.org/10.1016/0043-1354(95)00093-Z DOI: https://doi.org/10.1016/0043-1354(95)00093-Z
  76. Wani, P. A., Wahid, S., Khan, M. S. A., Rafi, N., & Wahid, N. (2019). Investigation of the role of chromium reductase for Cr (VI) reduction by Pseudomonas species isolated from Cr (VI) contaminated effluent. Biotechnology Research and Innovation, 3(1), 38-46.
  77. https://doi.org/10.1016/j.biori.2019.04.001 DOI: https://doi.org/10.1016/j.biori.2019.04.001
  78. WHO. Guideline for drinking water quality recommendations, (2010)(Vol. 1). Geneva: World Health Organization.
  79. Xiao, W., Ye, X., Yang, X., Zhu, Z., Sun, C., Zhang, Q., & Xu, P. (2017). Isolation and characterization of chromium (VI)-reducing Bacillus sp. FY1 and Arthrobacter sp. WZ2 and their bioremediation potential. Bioremediation Journal, 21(2), 100-108.
  80. https://doi.org/10.1080/10889868.2017.1282939 DOI: https://doi.org/10.1080/10889868.2017.1282939
  81. Zahoor, A., & Rehman, A. (2009). Isolation of Cr (VI) reducing bacteria from industrial effluents and their potential use in bioremediation of chromium containing wastewater. Journal of Environmental Sciences, 21(6), 814-820. https://doi.org/10.1016/S1001-0742(08)62346-3 DOI: https://doi.org/10.1016/S1001-0742(08)62346-3
  82. Zheng, X., Yuan, D., Li, Y., & Liu, C. (2019). Exploration of the reduction mechanism of Cr(VI) in anaerobic hydrogen fermenter. Environmental Pollution, 254, 113042. https://doi.org/10.1016/j.envpol.2019.113042 DOI: https://doi.org/10.1016/j.envpol.2019.113042
  83. Zhu, W., Yang, Z., Ma, Z., & Chai, L. (2008). Reduction of high concentrations of chromate by Leucobacter sp. CRB1 isolated from Changsha, China. World Journal of Microbiology and Biotechnology, 24(7), 991-996. https://doi.org/10.1007/s11274-007-9564-7 DOI: https://doi.org/10.1007/s11274-007-9564-7
  84. Zouboulis, A. I., Chai, X. L., & Katsoyiannis, I. A. (2004). The application of bioflocculants for the removal of humic acids from stabilized landfill leachates. Journal of Environmental Management, 70(1), 35-41. https://doi.org/10.1016/j.jenvman.2003.10.003 DOI: https://doi.org/10.1016/j.jenvman.2003.10.003