Bioremediation of chromium (VI) by a microbial consortium isolated from tannery effluents and their potential industrial application
Abstract
West Bengal has several leather industries and as such huge amount of leather are processed every year. The tannery effluents are discharged into the land and open water causing soil and water pollution respectively. Chromium is one of the most toxic inorganic contaminants which is well known for its carcinogenicity. Thus, our study focuses on investigating the bioremediation potential of common microflora isolated from tannery wastewater. In our study, Isolate 1 has the highest ability to reduce chromium (Cr6+) as compared to others. Isolate 4 has the highest protease, lipase and leather degradation activities. Isolate 1 shows the maximum keratinase activity making it an effective strain for keratinase production. Also, it has been found that pH 8 and temperature 40 °C was most suitable for keratinase production. Owing to the multidimensional ability of these two isolates, they were identified by 16S rRNA sequencing and it reveals that Isolate 1 and Isolate 4 belong to Bacillus cereus F4810/72 and Brevibacillus brevis F4810/72 respectively. Thus, this study establishes the role and efficiencies of these microorganisms in combatting pollution, particularly in the water bodies in which harmful chemicals leak regularly owing to improper waste management by various industries.
Please view correction statement: Corrigendum: Bioremediation of chromium (VI) by a microbial consortium isolated from tannery effluents and their potential industrial application
Keyword : effluent, groundwater, chromium, tannery, bioremediation, keratinase
How to Cite
Bhattacharjee, A., Chaudhuri, R., Pandey, P., & Mitra, A. K. (2021). Bioremediation of chromium (VI) by a microbial consortium isolated from tannery effluents and their potential industrial application. Journal of Environmental Engineering and Landscape Management, 29(4), 418–429. https://doi.org/10.3846/jeelm.2021.15762
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Adler, J., & Dahl, M. M. (1967). A method for measuring the motility of bacteria and for comparing random and non-random motility. Journal of General Microbiology, 46(2), 161–173. https://doi.org/10.1099/00221287-46-2-161
Al-Musharafi, S. K. (2016). Heavy metals in sewage treated effluents: Pollution and microbial bioremediation from arid regions. The Open Biotechnology Journal, 10(1), 352–362. https://doi.org/10.2174/1874070701610010352
Arias-Barreiro, C. R., Nishizaki, H., Okubo, K., Aoyama, I., & Mori, I. C. (2010). Ecotoxicological characterization of tannery wastewater in Dhaka, Bangladesh. Journal of Environmental Biology, 31(4), 471–475.
Ates, E., Orhon, D., & Tünay, O. (1997). Characterization of tannery wastewaters for pretreatment – Selected case studies. Water Science and Technology, 36(2–3), 217–223. https://doi.org/10.2166/wst.1997.0522
Ausubel, F. M. (1994). Preparation of genomic DNA from bacteria. Current Protocols in Molecular Biology, 2–4.
Basu, S., Dasgupta, M., & Chakraborty, B. (2014). Removal of chromium (VI) by Bacillus subtilis isolated from East Calcutta wetlands, West Bengal, India. International Journal of Bioscience, Biochemistry and Bioinformatics, 4(1), 7–10. https://doi.org/10.7763/IJBBB.2014.V4.300
Benazir, J. F., Suganthi, R., Rajvel, D., Pooja, M. P., & Mathithumilan, B. (2010). Bioremediation of chromium in tannery effluent by microbial consortia. African Journal of Biotechnology, 9(21), 3140–3143.
Bharagava, R. N., Saxena, G., Mulla, S. I., & Patel, D. K. (2018). Characterization and identification of recalcitrant organic pollutants (ROPs) in tannery wastewater and its phytotoxicity evaluation for environmental safety. Archives of Environmental Contamination and Toxicology, 75(2), 259–272. https://doi.org/10.1007/s00244-017-0490-x
Chatterjee, A., Bhattacharjee, A., & Mitra, A. K (2017). A study on the bioremediation ability of the common microflora isolated from tannery effluents. IOSR Journal of Environmental Science, Toxicology & Food Technology, 11(3), 104–114. https://doi.org/10.9790/2402-110303104114
Chen, L., Cai, Y., Zhou, G., Shi, X., Su, J., Chen, G., & Lin, K. (2014). Rapid Sanger sequencing of the 16S rRNA gene for identification of some common pathogens. PLoS ONE, 9(2), e88886. https://doi.org/10.1371/journal.pone.0088886
Chowdhury, M., Mostafa, M. G., Biswas, T. K., Mandal, A., & Saha, A. K. (2015). Characterization of the effluents from leather processing industries. Environmental Processes, 2(1), 173–187. https://doi.org/10.1007/s40710-015-0065-7
De La Luz-Pedro, A., Martínez Prior, E. F., López-Araiza, M. H., Jaime-Ferrer, S., Estrada-Monje, A., & Bañuelos, J. A. (2019). Pollutant removal from wastewater at different stages of the tanning process by electrocoagulation. Journal of Chemistry, 2019, 8162931. https://doi.org/10.1155/2019/8162931
Elangovan, R., Philip, L., & Chandraraj, K. (2010). Hexavalent chromium reduction by free and immobilized cell-free extract of Arthrobacter rhombi-RE. Applied Biochemistry and Biotechnology, 160, 81–97. https://doi.org/10.1007/s12010-008-8515-6
El-Refai, H. A., AbdelNaby, M. A., Gaballa, A., El-Araby, M. H., & Fattah, A. A. (2005). Improvement of the newly isolated Bacillus pumilus FH9 keratinolytic activity. Process Biochemistry, 40(7), 2325–2332. https://doi.org/10.1016/j.procbio.2004.09.006
Espinoza-Quiñones, F. R., Fornari, M. M., Módenes, A. N., Palácio, S. M., da Silva Jr, F. G., Szymanski, N., Kroumov, A. D., & Trigueros, D. E. (2009). Pollutant removal from tannery effluent by electrocoagulation. Chemical Engineering Journal, 151(1–3), 59–65. https://doi.org/10.1016/j.cej.2009.01.043
Fahim, N. F., Barsoum, B. N., Eid, A. E., & Khalil, M. S. (2006). Removal of chromium(III) from tannery wastewater using activated carbon from sugar industrial waste. Journal of Hazardous Materials, 136(2), 303–309. https://doi.org/10.1016/j.jhazmat.2005.12.014
Fernández, P. M., Viñarta, S. C., Bernal, A. R., Cruz, E. L., & Figueroa, L. I. C. (2018). Bioremediation strategies for chromium removal: Current research, scale-up approach and future perspectives. Chemosphere, 208, 139–148. https://doi.org/10.1016/j.chemosphere.2018.05.166
Garg, S. K., Tripathi, M., & Srinath, T. (2012). Strategies for chromium bioremediation of tannery effluent. In D. M. Whitacre (Ed.), Reviews of environmental contamination and toxicology: Vol. 217. Reviews of environmental contamination and toxicology (Continuation of residue reviews) (pp. 75–140). Springer. https://doi.org/10.1007/978-1-4614-2329-4_2
Gupta, K., Gaumat, S., & Mishra, K. (2011). Chromium accumulation in submerged aquatic plants treated with tannery effluent at Kanpur, India. Journal of Environmental Biology, 32(5), 591–597.
Hassen, A. S., & Woldeamanuale, T. B. (2017). Evaluation and characterization of Tannery Wastewater in each process at batu and modjo tannery, Ethiopia. International Journal of Rural Development, Environment and Health Research, 1(3), 17–26.
Hess, H. H., Lees, M. B., & Derr, J. E. (1978). A linear Lowry-Folin assay for both water-soluble and sodium dodecyl sulfate-solubilized proteins. Analytical Biochemistry, 85(1), 295–300. https://doi.org/10.1016/0003-2697(78)90304-4
Igiri, B. E., Okoduwa, S. I., Idoko, G. O., Akabuogu, E. P., Adeyi, A. O., & Ejiogu, I. K. (2018). Toxicity and bioremediation of heavy metals contaminated ecosystem from tannery wastewater: A review. Journal of Toxicology, 2018, 2568038. https://doi.org/10.1155/2018/2568038
Iyer, G. V., Mastorakis, N. E., & Theologou, A. I. (2006, May 8–10). Assessment of pollution load from unsafe chromium leather tanneries in India. In Proceedings of the 2006 IASME/WSEAS International Conference on Energy & Environmental Systems (pp. 496–505), Chalkida, Greece.
Jahan, M., Akhtar, N., Khan, N., Roy, C., Islam, R., & Nurunnabi, M. (2015). Characterization of tannery wastewater and its treatment by aquatic macrophytes and algae. Bangladesh Journal of Scientific and Industrial Research, 49(4), 233–242. https://doi.org/10.3329/bjsir.v49i4.22626
Jaouadi, N. Z., Rekik, H., Badis, A., Trabelsi, S., Belhoul, M., Yahiaoui, A. B., Aicha, H. B., Toumi, A., Bejar, S., & Jaouadi, B. (2013). Biochemical and molecular characterization of a serine keratinase from Brevibacillus brevis US575 with promising keratin-biodegradation and hide-dehairing activities. PLoS ONE, 8(10), e76722. https://doi.org/10.1371/journal.pone.0076722
Jaouadi, N. Z., Rekik, H., Badis, A., Trabelsi, S., Belhoul, M., Hila, C. G., Irmani, A., Khemir, H., Toumi, A., Bejar, S., & Jaouadi, B. (2017). The promising keratin-biodegradation and hide-dehairing activities of the keratinase KERUS from Brevibacillus brevis strain US575. In Advances in Science, Technology & Innovation. Recent Advances in Environmental Science from the Euro-Mediterranean and Surrounding Regions (pp. 133–135). Springer, Cham. https://doi.org/10.1007/978-3-319-70548-4_45
Jin, H. S., Park, S. Y., Kim, K., Lee, Y. J., Nam, G. W., Kang, N. J., & Lee, D. W. (2017). Development of a keratinase activity assay using recombinant chicken feather keratin substrates. PLoS ONE, 12(2), e0172712. https://doi.org/10.1371/journal.pone.0172712
Kanimozhi, K., Devairrakam, E. W. J., & Jegadeeshkumar, D. (2013). Decolorization of Leather effluent by lipase producing Bacillus sp. Journal of Academia and Industrial Research, 1(12), 813–815.
Kapoor, A., & Viraraghavan, T. (1995). Fungal biosorption – an alternative treatment option for heavy metal bearing wastewaters: A review. Bioresource Technology, 53(3), 195–206.
Kumar, A. R., & Riyazuddin, P. (2010). Chromium speciation in groundwater of a tannery polluted area of Chennai City, India. Environmental Monitoring and Assessment, 160(1–4), 579–591. https://doi.org/10.1007/s10661-008-0720-9
Kumari, V., Yadav, A., Haq, I., Kumar, S., Bharagava, R. N., Singh, S. K., & Raj, A. (2016). Genotoxicity evaluation of tannery effluent treated with newly isolated hexavalent chromium reducing Bacillus cereus. Journal of Environmental Management, 183, 204–211. https://doi.org/10.1016/j.jenvman.2016.08.017
Leung, R., Venus, C., Zeng, T., & Tsopmo, A. (2018). Structure-function relationships of hydroxyl radical scavenging and chromium-VI reducing cysteine-tripeptides derived from rye secalin. Food Chemistry, 254, 165–169. https://doi.org/10.1016/j.foodchem.2018.01.190
Mallick, N., & Rai, L. C. (1994). Removal of inorganic ions from wastewaters by immobilized microalgae. World Journal of Microbiology and Biotechnology, 10(4), 439–443. https://doi.org/10.1007/BF00144469
Marzan, L. W., Hossain, M., Mina, S. A., Akter, Y., & Chowdhury, A. M. A. (2017). Isolation and biochemical characterization of heavy-metal resistant bacteria from tannery effluent in Chittagong city, Bangladesh: Bioremediation viewpoint. The Egyptian Journal of Aquatic Research, 43(1), 65–74. https://doi.org/10.1016/j.ejar.2016.11.002
McLean, J., & Beveridge, T. J. (2001). Chromate reduction by a pseudomonad isolated from a site contaminated with chromated copper arsenate. Applied and Environmental Microbiology, 67(3), 1076–1084. https://doi.org/10.1128/AEM.67.3.1076-1084.2001
Mohanty, M., & Patra, H. K. (2011). Attenuation of chromium toxicity by bioremediation technology. In D. M. Whitacre (Ed.), Reviews of environmental contamination and toxicology: Vol. 210. Reviews of environmental contamination and toxicology (pp. 1–34). Springer. https://doi.org/10.1007/978-1-4419-7615-4_1
Mukherjee, K., Tribedi, P., Chowdhury, A., Ray, T., Joardar, A., Giri, S., & Sil, A. K. (2011). Isolation of a Pseudomonas aeruginosa strain from soil that can degrade polyurethane diol. Biodegradation, 22(2), 377–388. https://doi.org/10.1007/s10532-010-9409-1
Mythili, K., & Karthikeyan, B. (2011). Bioremediation of Cr (VI) from Tannery effluent using Bacillus spp and Staphylococcus spp. International Multidisciplinary Research Journal, 1(6), 38–41.
Oliveira, H. (2012). Chromium as an environmental pollutant: Insights on induced plant toxicity. Journal of Botany, 2012, 375843. https://doi.org/10.1155/2012/375843
Pandi, A., Kuppuswami, G. M., Ramudu, K. N., & Palanivel, S. (2019). A sustainable approach for degradation of leather dyes by a new fungal laccase. Journal of Cleaner Production, 211, 590–597. https://doi.org/10.1016/j.jclepro.2018.11.048
Park, D. (2007). Genomic DNA isolation from different biological materials. In E. Hilario & J. Mackay (Eds.), Methods in molecular biology: Vol. 353. Protocols for nucleic acid analysis by nonradioactive probes (pp. 3–13). Humana Press. https://doi.org/10.1385/1-59745-229-7:3
Pescuma, M., Hébert, E. M., Bru, E., de Valdez, G. F., & Mozzi, F. (2012). Diversity in growth and protein degradation by dairy relevant lactic acid bacteria species in reconstituted whey. The Journal of Dairy Research, 79(2), 201–208. https://doi.org/10.1017/S0022029912000040
Pillai, P., Mandge, S., & Archana, G. (2011). Statistical optimization of production and tannery applications of a keratinolytic serine protease from Bacillus subtilis P13. Process Biochemistry, 46(5), 1110–1117. https://doi.org/10.1016/j.procbio.2011.01.030
Raman, N. M., Asokan, S., Sundari, N. S., & Ramasamy, S. (2018). Bioremediation of chromium(VI) by Stenotrophomonas maltophilia isolated from tannery effluent. International Journal of Environmental Science and Technology, 15(1), 207–216. https://doi.org/10.1007/s13762-017-1378-z
Reiner, K. (2010). Catalase test protocol. American Society for Microbiology.
Romero-Gonzalez, J., Peralta-Videa, J. R., Rodriguez, E., Delgado, M., & Gardea-Torresdey, J. L. (2006). Potential of Agave lechuguilla biomass for Cr(III) removal from aqueous solutions: Thermodynamic studies. Bioresource Technology, 97(1), 178–182. https://doi.org/10.1016/j.biortech.2005.01.037
Sanjay, M. S., Sudarsanam, D., Raj, G. A., & Baskar, K. (2020). Isolation and identification of chromium reducing bacteria from tannery effluent. Journal of King Saud University – Science, 32(1), 265–271. https://doi.org/10.1016/j.jksus.2018.05.001
Saranraj, P., & Sujitha, D. (2013). Microbial bioremediation of chromium in tannery effluent: A review. International Journal of Microbiological Research, 4(3), 305–320.
Savita, K., & Archana, P. (2014). Screening of keratinase producers from leather. Journal of Environmental Research and Development, 8(3A), 639.
Sharma, S., & Adholeya, A. (2011). Detoxification and accumulation of chromium from tannery effluent and spent chrome effluent by Paecilomyces lilacinus fungi. International Biodeterioration & Biodegradation, 65(2), 309–317. https://doi.org/10.1016/j.ibiod.2010.12.003
Sharma, S., & Malaviya, P. (2014). Bioremediation of tannery wastewater by chromium resistant fungal isolate Fusarium chlamydosporium SPFS2-g. Current World Environment, 9(3), 721. https://doi.org/10.12944/CWE.9.3.21
Sharma, S., & Malaviya, P. (2016). Bioremediation of tannery wastewater by chromium resistant novel fungal consortium. Ecological Engineering, 91, 419–425. https://doi.org/10.1016/j.ecoleng.2016.03.005
Shields, P., & Cathcart, L. (2010). Oxidase test protocol. Library. In ASM Conference for Undergraduate Educators (pp. 1–5). American Society for Microbiology.
Singh, N., Verma, T., & Gaur, R. (2013). Detoxification of hexavalent chromium by an indigenous facultative anaerobic Bacillus cereus strain isolated from tannery effluent. African Journal of Biotechnology, 12(10), 1091–1103.
Smith, W. A., Apel, W. A., Petersen, J. N., & Peyton, B. M. (2002). Effect of carbon and energy source on bacterial chromate reduction. Bioremediation Journal, 6(3), 205–215. https://doi.org/10.1080/10889860290777567
Srinath, T., Khare, S., & Ramteke, P. W. (2001). Isolation of hexavalent chromium-reducing Cr-tolerant facultative anaerobes from tannery effluent. The Journal of General and Applied Microbiology, 47(6), 307–312. https://doi.org/10.2323/jgam.47.307
Sumathi, K. M. S., Mahimairaja, S., & Naidu, R. (2005). Use of low-cost biological wastes and vermiculite for removal of chromium from tannery effluent. Bioresource Technology, 96(3), 309–316. https://doi.org/10.1016/j.biortech.2004.04.015
Thakur, I. S., & Srivastava, S. (2011). Bioremediation and bioconversion of chromium and pentachlorophenol in tannery effluent by microorganisms. International Journal of Technology, 2(3), 224–233.
Tripathi, M., Vikram, S., Jain, R. K., & Garg, S. K. (2011). Isolation and growth characteristics of chromium(VI) and pentachlorophenol tolerant bacterial isolate from treated tannery effluent for its possible use in simultaneous bioremediation. Indian Journal of Microbiology, 51(1), 61–69. https://doi.org/10.1007/s12088-011-0089-2
Trivedi, M., Branton, A., Trivedi, D., Nayak, G., Gangwar, M., & Jana, S. (2015). Agronomic characteristics, growth analysis, and yield response of biofield treated mustard, cowpea, horse gram, and groundnuts. International Journal of Genetics and Genomics, 6(3), 74–80. https://doi.org/10.11648/j.ijgg.20150306.13
Vajpayee, P., Rai, U. N., Ali, M. B., Tripathi, R. D., Yadav, V., Sinha, S., & Singh, S. N. (2001). Chromium-induced physiologic changes in Vallisneria spiralis L. and its role in phytoremediation of tannery. Bulletin of Environmental Contamination and Toxicology, 67, 246–256. https://doi.org/10.1007/s001280117
Verma, N., Batta, S., & Rehal, R. (1995). Studies on some cyanobacteria for the selection of bioindicators and bioscavengers of chromium metal ions for industrial waste waters. International Journal of Environmental Studies, 47(3–4), 211–215. https://doi.org/10.1080/00207239508710961
Verma, T., Srinath, T., Gadpayle, R. U., Ramteke, P. W., Hans, R. K., & Garg, S. K. (2001). Chromate tolerant bacteria isolated from tannery effluent. Bioresource Technology, 78(1), 31–35. https://doi.org/10.1016/S0960-8524(00)00168-1
Vijayaraj, A. S., Mohandass, C., Joshi, D., & Rajput, N. (2018). Effective bioremediation and toxicity assessment of tannery wastewaters treated with indigenous bacteria. 3 Biotech, 8(10), 1–11. https://doi.org/10.1007/s13205-018-1444-3
Viti, C., Pace, A., & Giovannetti, L. (2003). Characterization of Cr(VI)-resistant bacteria isolated from chromium-contaminated soil by tannery activity. Current Microbiology, 46(1), 0001–0005. https://doi.org/10.1007/s00284-002-3800-z
Yang, W., Yan, L., Wu, C., Zhao, X., & Tang, J. (2014). Fungal invasion of epithelial cells. Microbiological Research, 169(11), 803–810. https://doi.org/10.1016/j.micres.2014.02.013
Wang, B., Rezenom, Y. H., Cho, K. C., Tran, J. L., Lee, D. G., Russell, D. H., Gill, J. J., Young, R., & Chu, K. H. (2014). Cultivation of lipid-producing bacteria with lignocellulosic biomass: Effects of inhibitory compounds of lignocellulosic hydrolysates. Bioresource Technology, 161, 162–170. https://doi.org/10.1016/j.biortech.2014.02.133
Wang, J., Gao, Q., Zhang, H., & Bao, J. (2016). Inhibitor degradation and lipid accumulation potentials of oleaginous yeast Trichosporon cutaneum using lignocellulose feedstock. Bioresource Technology, 218, 892–901. https://doi.org/10.1016/j.biortech.2016.06.130
Waterborg, J. H., & Matthews, H. R. (1984). The Lowry method for protein quantitation. In J. M. Walker (Ed.), Methods in molecular biology: Vol. 1. Proteins (pp. 1–3). Springer. https://doi.org/10.1385/0-89603-062-8:1
Woo, P. C. Y., Lau, S. K. P., Teng, J. L. L., Tse, H., & Yuen, K. Y. (2008). Then and now: Use of 16S rDNA gene sequencing for bacterial identification and discovery of novel bacteria in clinical microbiology laboratories. Clinical Microbiology and Infection, 14(10), 908–934. https://doi.org/10.1111/j.1469-0691.2008.02070.x
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
Zhao, C., Yang, Q., Chen, W., & Teng, B. (2012). Removal of hexavalent chromium in tannery wastewater by Bacillus cereus. Canadian Journal of Microbiology, 58(1), 23–28. https://doi.org/10.1139/w11-096
Al-Musharafi, S. K. (2016). Heavy metals in sewage treated effluents: Pollution and microbial bioremediation from arid regions. The Open Biotechnology Journal, 10(1), 352–362. https://doi.org/10.2174/1874070701610010352
Arias-Barreiro, C. R., Nishizaki, H., Okubo, K., Aoyama, I., & Mori, I. C. (2010). Ecotoxicological characterization of tannery wastewater in Dhaka, Bangladesh. Journal of Environmental Biology, 31(4), 471–475.
Ates, E., Orhon, D., & Tünay, O. (1997). Characterization of tannery wastewaters for pretreatment – Selected case studies. Water Science and Technology, 36(2–3), 217–223. https://doi.org/10.2166/wst.1997.0522
Ausubel, F. M. (1994). Preparation of genomic DNA from bacteria. Current Protocols in Molecular Biology, 2–4.
Basu, S., Dasgupta, M., & Chakraborty, B. (2014). Removal of chromium (VI) by Bacillus subtilis isolated from East Calcutta wetlands, West Bengal, India. International Journal of Bioscience, Biochemistry and Bioinformatics, 4(1), 7–10. https://doi.org/10.7763/IJBBB.2014.V4.300
Benazir, J. F., Suganthi, R., Rajvel, D., Pooja, M. P., & Mathithumilan, B. (2010). Bioremediation of chromium in tannery effluent by microbial consortia. African Journal of Biotechnology, 9(21), 3140–3143.
Bharagava, R. N., Saxena, G., Mulla, S. I., & Patel, D. K. (2018). Characterization and identification of recalcitrant organic pollutants (ROPs) in tannery wastewater and its phytotoxicity evaluation for environmental safety. Archives of Environmental Contamination and Toxicology, 75(2), 259–272. https://doi.org/10.1007/s00244-017-0490-x
Chatterjee, A., Bhattacharjee, A., & Mitra, A. K (2017). A study on the bioremediation ability of the common microflora isolated from tannery effluents. IOSR Journal of Environmental Science, Toxicology & Food Technology, 11(3), 104–114. https://doi.org/10.9790/2402-110303104114
Chen, L., Cai, Y., Zhou, G., Shi, X., Su, J., Chen, G., & Lin, K. (2014). Rapid Sanger sequencing of the 16S rRNA gene for identification of some common pathogens. PLoS ONE, 9(2), e88886. https://doi.org/10.1371/journal.pone.0088886
Chowdhury, M., Mostafa, M. G., Biswas, T. K., Mandal, A., & Saha, A. K. (2015). Characterization of the effluents from leather processing industries. Environmental Processes, 2(1), 173–187. https://doi.org/10.1007/s40710-015-0065-7
De La Luz-Pedro, A., Martínez Prior, E. F., López-Araiza, M. H., Jaime-Ferrer, S., Estrada-Monje, A., & Bañuelos, J. A. (2019). Pollutant removal from wastewater at different stages of the tanning process by electrocoagulation. Journal of Chemistry, 2019, 8162931. https://doi.org/10.1155/2019/8162931
Elangovan, R., Philip, L., & Chandraraj, K. (2010). Hexavalent chromium reduction by free and immobilized cell-free extract of Arthrobacter rhombi-RE. Applied Biochemistry and Biotechnology, 160, 81–97. https://doi.org/10.1007/s12010-008-8515-6
El-Refai, H. A., AbdelNaby, M. A., Gaballa, A., El-Araby, M. H., & Fattah, A. A. (2005). Improvement of the newly isolated Bacillus pumilus FH9 keratinolytic activity. Process Biochemistry, 40(7), 2325–2332. https://doi.org/10.1016/j.procbio.2004.09.006
Espinoza-Quiñones, F. R., Fornari, M. M., Módenes, A. N., Palácio, S. M., da Silva Jr, F. G., Szymanski, N., Kroumov, A. D., & Trigueros, D. E. (2009). Pollutant removal from tannery effluent by electrocoagulation. Chemical Engineering Journal, 151(1–3), 59–65. https://doi.org/10.1016/j.cej.2009.01.043
Fahim, N. F., Barsoum, B. N., Eid, A. E., & Khalil, M. S. (2006). Removal of chromium(III) from tannery wastewater using activated carbon from sugar industrial waste. Journal of Hazardous Materials, 136(2), 303–309. https://doi.org/10.1016/j.jhazmat.2005.12.014
Fernández, P. M., Viñarta, S. C., Bernal, A. R., Cruz, E. L., & Figueroa, L. I. C. (2018). Bioremediation strategies for chromium removal: Current research, scale-up approach and future perspectives. Chemosphere, 208, 139–148. https://doi.org/10.1016/j.chemosphere.2018.05.166
Garg, S. K., Tripathi, M., & Srinath, T. (2012). Strategies for chromium bioremediation of tannery effluent. In D. M. Whitacre (Ed.), Reviews of environmental contamination and toxicology: Vol. 217. Reviews of environmental contamination and toxicology (Continuation of residue reviews) (pp. 75–140). Springer. https://doi.org/10.1007/978-1-4614-2329-4_2
Gupta, K., Gaumat, S., & Mishra, K. (2011). Chromium accumulation in submerged aquatic plants treated with tannery effluent at Kanpur, India. Journal of Environmental Biology, 32(5), 591–597.
Hassen, A. S., & Woldeamanuale, T. B. (2017). Evaluation and characterization of Tannery Wastewater in each process at batu and modjo tannery, Ethiopia. International Journal of Rural Development, Environment and Health Research, 1(3), 17–26.
Hess, H. H., Lees, M. B., & Derr, J. E. (1978). A linear Lowry-Folin assay for both water-soluble and sodium dodecyl sulfate-solubilized proteins. Analytical Biochemistry, 85(1), 295–300. https://doi.org/10.1016/0003-2697(78)90304-4
Igiri, B. E., Okoduwa, S. I., Idoko, G. O., Akabuogu, E. P., Adeyi, A. O., & Ejiogu, I. K. (2018). Toxicity and bioremediation of heavy metals contaminated ecosystem from tannery wastewater: A review. Journal of Toxicology, 2018, 2568038. https://doi.org/10.1155/2018/2568038
Iyer, G. V., Mastorakis, N. E., & Theologou, A. I. (2006, May 8–10). Assessment of pollution load from unsafe chromium leather tanneries in India. In Proceedings of the 2006 IASME/WSEAS International Conference on Energy & Environmental Systems (pp. 496–505), Chalkida, Greece.
Jahan, M., Akhtar, N., Khan, N., Roy, C., Islam, R., & Nurunnabi, M. (2015). Characterization of tannery wastewater and its treatment by aquatic macrophytes and algae. Bangladesh Journal of Scientific and Industrial Research, 49(4), 233–242. https://doi.org/10.3329/bjsir.v49i4.22626
Jaouadi, N. Z., Rekik, H., Badis, A., Trabelsi, S., Belhoul, M., Yahiaoui, A. B., Aicha, H. B., Toumi, A., Bejar, S., & Jaouadi, B. (2013). Biochemical and molecular characterization of a serine keratinase from Brevibacillus brevis US575 with promising keratin-biodegradation and hide-dehairing activities. PLoS ONE, 8(10), e76722. https://doi.org/10.1371/journal.pone.0076722
Jaouadi, N. Z., Rekik, H., Badis, A., Trabelsi, S., Belhoul, M., Hila, C. G., Irmani, A., Khemir, H., Toumi, A., Bejar, S., & Jaouadi, B. (2017). The promising keratin-biodegradation and hide-dehairing activities of the keratinase KERUS from Brevibacillus brevis strain US575. In Advances in Science, Technology & Innovation. Recent Advances in Environmental Science from the Euro-Mediterranean and Surrounding Regions (pp. 133–135). Springer, Cham. https://doi.org/10.1007/978-3-319-70548-4_45
Jin, H. S., Park, S. Y., Kim, K., Lee, Y. J., Nam, G. W., Kang, N. J., & Lee, D. W. (2017). Development of a keratinase activity assay using recombinant chicken feather keratin substrates. PLoS ONE, 12(2), e0172712. https://doi.org/10.1371/journal.pone.0172712
Kanimozhi, K., Devairrakam, E. W. J., & Jegadeeshkumar, D. (2013). Decolorization of Leather effluent by lipase producing Bacillus sp. Journal of Academia and Industrial Research, 1(12), 813–815.
Kapoor, A., & Viraraghavan, T. (1995). Fungal biosorption – an alternative treatment option for heavy metal bearing wastewaters: A review. Bioresource Technology, 53(3), 195–206.
Kumar, A. R., & Riyazuddin, P. (2010). Chromium speciation in groundwater of a tannery polluted area of Chennai City, India. Environmental Monitoring and Assessment, 160(1–4), 579–591. https://doi.org/10.1007/s10661-008-0720-9
Kumari, V., Yadav, A., Haq, I., Kumar, S., Bharagava, R. N., Singh, S. K., & Raj, A. (2016). Genotoxicity evaluation of tannery effluent treated with newly isolated hexavalent chromium reducing Bacillus cereus. Journal of Environmental Management, 183, 204–211. https://doi.org/10.1016/j.jenvman.2016.08.017
Leung, R., Venus, C., Zeng, T., & Tsopmo, A. (2018). Structure-function relationships of hydroxyl radical scavenging and chromium-VI reducing cysteine-tripeptides derived from rye secalin. Food Chemistry, 254, 165–169. https://doi.org/10.1016/j.foodchem.2018.01.190
Mallick, N., & Rai, L. C. (1994). Removal of inorganic ions from wastewaters by immobilized microalgae. World Journal of Microbiology and Biotechnology, 10(4), 439–443. https://doi.org/10.1007/BF00144469
Marzan, L. W., Hossain, M., Mina, S. A., Akter, Y., & Chowdhury, A. M. A. (2017). Isolation and biochemical characterization of heavy-metal resistant bacteria from tannery effluent in Chittagong city, Bangladesh: Bioremediation viewpoint. The Egyptian Journal of Aquatic Research, 43(1), 65–74. https://doi.org/10.1016/j.ejar.2016.11.002
McLean, J., & Beveridge, T. J. (2001). Chromate reduction by a pseudomonad isolated from a site contaminated with chromated copper arsenate. Applied and Environmental Microbiology, 67(3), 1076–1084. https://doi.org/10.1128/AEM.67.3.1076-1084.2001
Mohanty, M., & Patra, H. K. (2011). Attenuation of chromium toxicity by bioremediation technology. In D. M. Whitacre (Ed.), Reviews of environmental contamination and toxicology: Vol. 210. Reviews of environmental contamination and toxicology (pp. 1–34). Springer. https://doi.org/10.1007/978-1-4419-7615-4_1
Mukherjee, K., Tribedi, P., Chowdhury, A., Ray, T., Joardar, A., Giri, S., & Sil, A. K. (2011). Isolation of a Pseudomonas aeruginosa strain from soil that can degrade polyurethane diol. Biodegradation, 22(2), 377–388. https://doi.org/10.1007/s10532-010-9409-1
Mythili, K., & Karthikeyan, B. (2011). Bioremediation of Cr (VI) from Tannery effluent using Bacillus spp and Staphylococcus spp. International Multidisciplinary Research Journal, 1(6), 38–41.
Oliveira, H. (2012). Chromium as an environmental pollutant: Insights on induced plant toxicity. Journal of Botany, 2012, 375843. https://doi.org/10.1155/2012/375843
Pandi, A., Kuppuswami, G. M., Ramudu, K. N., & Palanivel, S. (2019). A sustainable approach for degradation of leather dyes by a new fungal laccase. Journal of Cleaner Production, 211, 590–597. https://doi.org/10.1016/j.jclepro.2018.11.048
Park, D. (2007). Genomic DNA isolation from different biological materials. In E. Hilario & J. Mackay (Eds.), Methods in molecular biology: Vol. 353. Protocols for nucleic acid analysis by nonradioactive probes (pp. 3–13). Humana Press. https://doi.org/10.1385/1-59745-229-7:3
Pescuma, M., Hébert, E. M., Bru, E., de Valdez, G. F., & Mozzi, F. (2012). Diversity in growth and protein degradation by dairy relevant lactic acid bacteria species in reconstituted whey. The Journal of Dairy Research, 79(2), 201–208. https://doi.org/10.1017/S0022029912000040
Pillai, P., Mandge, S., & Archana, G. (2011). Statistical optimization of production and tannery applications of a keratinolytic serine protease from Bacillus subtilis P13. Process Biochemistry, 46(5), 1110–1117. https://doi.org/10.1016/j.procbio.2011.01.030
Raman, N. M., Asokan, S., Sundari, N. S., & Ramasamy, S. (2018). Bioremediation of chromium(VI) by Stenotrophomonas maltophilia isolated from tannery effluent. International Journal of Environmental Science and Technology, 15(1), 207–216. https://doi.org/10.1007/s13762-017-1378-z
Reiner, K. (2010). Catalase test protocol. American Society for Microbiology.
Romero-Gonzalez, J., Peralta-Videa, J. R., Rodriguez, E., Delgado, M., & Gardea-Torresdey, J. L. (2006). Potential of Agave lechuguilla biomass for Cr(III) removal from aqueous solutions: Thermodynamic studies. Bioresource Technology, 97(1), 178–182. https://doi.org/10.1016/j.biortech.2005.01.037
Sanjay, M. S., Sudarsanam, D., Raj, G. A., & Baskar, K. (2020). Isolation and identification of chromium reducing bacteria from tannery effluent. Journal of King Saud University – Science, 32(1), 265–271. https://doi.org/10.1016/j.jksus.2018.05.001
Saranraj, P., & Sujitha, D. (2013). Microbial bioremediation of chromium in tannery effluent: A review. International Journal of Microbiological Research, 4(3), 305–320.
Savita, K., & Archana, P. (2014). Screening of keratinase producers from leather. Journal of Environmental Research and Development, 8(3A), 639.
Sharma, S., & Adholeya, A. (2011). Detoxification and accumulation of chromium from tannery effluent and spent chrome effluent by Paecilomyces lilacinus fungi. International Biodeterioration & Biodegradation, 65(2), 309–317. https://doi.org/10.1016/j.ibiod.2010.12.003
Sharma, S., & Malaviya, P. (2014). Bioremediation of tannery wastewater by chromium resistant fungal isolate Fusarium chlamydosporium SPFS2-g. Current World Environment, 9(3), 721. https://doi.org/10.12944/CWE.9.3.21
Sharma, S., & Malaviya, P. (2016). Bioremediation of tannery wastewater by chromium resistant novel fungal consortium. Ecological Engineering, 91, 419–425. https://doi.org/10.1016/j.ecoleng.2016.03.005
Shields, P., & Cathcart, L. (2010). Oxidase test protocol. Library. In ASM Conference for Undergraduate Educators (pp. 1–5). American Society for Microbiology.
Singh, N., Verma, T., & Gaur, R. (2013). Detoxification of hexavalent chromium by an indigenous facultative anaerobic Bacillus cereus strain isolated from tannery effluent. African Journal of Biotechnology, 12(10), 1091–1103.
Smith, W. A., Apel, W. A., Petersen, J. N., & Peyton, B. M. (2002). Effect of carbon and energy source on bacterial chromate reduction. Bioremediation Journal, 6(3), 205–215. https://doi.org/10.1080/10889860290777567
Srinath, T., Khare, S., & Ramteke, P. W. (2001). Isolation of hexavalent chromium-reducing Cr-tolerant facultative anaerobes from tannery effluent. The Journal of General and Applied Microbiology, 47(6), 307–312. https://doi.org/10.2323/jgam.47.307
Sumathi, K. M. S., Mahimairaja, S., & Naidu, R. (2005). Use of low-cost biological wastes and vermiculite for removal of chromium from tannery effluent. Bioresource Technology, 96(3), 309–316. https://doi.org/10.1016/j.biortech.2004.04.015
Thakur, I. S., & Srivastava, S. (2011). Bioremediation and bioconversion of chromium and pentachlorophenol in tannery effluent by microorganisms. International Journal of Technology, 2(3), 224–233.
Tripathi, M., Vikram, S., Jain, R. K., & Garg, S. K. (2011). Isolation and growth characteristics of chromium(VI) and pentachlorophenol tolerant bacterial isolate from treated tannery effluent for its possible use in simultaneous bioremediation. Indian Journal of Microbiology, 51(1), 61–69. https://doi.org/10.1007/s12088-011-0089-2
Trivedi, M., Branton, A., Trivedi, D., Nayak, G., Gangwar, M., & Jana, S. (2015). Agronomic characteristics, growth analysis, and yield response of biofield treated mustard, cowpea, horse gram, and groundnuts. International Journal of Genetics and Genomics, 6(3), 74–80. https://doi.org/10.11648/j.ijgg.20150306.13
Vajpayee, P., Rai, U. N., Ali, M. B., Tripathi, R. D., Yadav, V., Sinha, S., & Singh, S. N. (2001). Chromium-induced physiologic changes in Vallisneria spiralis L. and its role in phytoremediation of tannery. Bulletin of Environmental Contamination and Toxicology, 67, 246–256. https://doi.org/10.1007/s001280117
Verma, N., Batta, S., & Rehal, R. (1995). Studies on some cyanobacteria for the selection of bioindicators and bioscavengers of chromium metal ions for industrial waste waters. International Journal of Environmental Studies, 47(3–4), 211–215. https://doi.org/10.1080/00207239508710961
Verma, T., Srinath, T., Gadpayle, R. U., Ramteke, P. W., Hans, R. K., & Garg, S. K. (2001). Chromate tolerant bacteria isolated from tannery effluent. Bioresource Technology, 78(1), 31–35. https://doi.org/10.1016/S0960-8524(00)00168-1
Vijayaraj, A. S., Mohandass, C., Joshi, D., & Rajput, N. (2018). Effective bioremediation and toxicity assessment of tannery wastewaters treated with indigenous bacteria. 3 Biotech, 8(10), 1–11. https://doi.org/10.1007/s13205-018-1444-3
Viti, C., Pace, A., & Giovannetti, L. (2003). Characterization of Cr(VI)-resistant bacteria isolated from chromium-contaminated soil by tannery activity. Current Microbiology, 46(1), 0001–0005. https://doi.org/10.1007/s00284-002-3800-z
Yang, W., Yan, L., Wu, C., Zhao, X., & Tang, J. (2014). Fungal invasion of epithelial cells. Microbiological Research, 169(11), 803–810. https://doi.org/10.1016/j.micres.2014.02.013
Wang, B., Rezenom, Y. H., Cho, K. C., Tran, J. L., Lee, D. G., Russell, D. H., Gill, J. J., Young, R., & Chu, K. H. (2014). Cultivation of lipid-producing bacteria with lignocellulosic biomass: Effects of inhibitory compounds of lignocellulosic hydrolysates. Bioresource Technology, 161, 162–170. https://doi.org/10.1016/j.biortech.2014.02.133
Wang, J., Gao, Q., Zhang, H., & Bao, J. (2016). Inhibitor degradation and lipid accumulation potentials of oleaginous yeast Trichosporon cutaneum using lignocellulose feedstock. Bioresource Technology, 218, 892–901. https://doi.org/10.1016/j.biortech.2016.06.130
Waterborg, J. H., & Matthews, H. R. (1984). The Lowry method for protein quantitation. In J. M. Walker (Ed.), Methods in molecular biology: Vol. 1. Proteins (pp. 1–3). Springer. https://doi.org/10.1385/0-89603-062-8:1
Woo, P. C. Y., Lau, S. K. P., Teng, J. L. L., Tse, H., & Yuen, K. Y. (2008). Then and now: Use of 16S rDNA gene sequencing for bacterial identification and discovery of novel bacteria in clinical microbiology laboratories. Clinical Microbiology and Infection, 14(10), 908–934. https://doi.org/10.1111/j.1469-0691.2008.02070.x
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
Zhao, C., Yang, Q., Chen, W., & Teng, B. (2012). Removal of hexavalent chromium in tannery wastewater by Bacillus cereus. Canadian Journal of Microbiology, 58(1), 23–28. https://doi.org/10.1139/w11-096