Chromium bioremediation of batik industrial wastewater using a consortium of sulfate-reducing bacteria from forested wetland soil
DOI:
https://doi.org/10.15243/jdmlm.2022.093.3511Keywords:
batch bioremediation, biofilm, continuous bioremediation, molasses, zeoliteAbstract
Chromium pollutants in textile wastewater can be removed by bioremediation using sulfate-reducing bacteria (SRB) from forested wetland soil. Biostimulation of carbon sources in the form of molasses and a supporting material in the form of zeolite to trap bacteria and create biofilms can improve the ability of SRB to bioremediate chromium. The batch bioremediation technique was further examined by including molasses, a combination of molasses and zeolite, and SRB, which has been adapted to acclimatize wastewater that is diluted two times. Adaptive SRB aged 7 days, which had reached the exponential growth phase, showed optimal bioremediation activity when molasses and zeolite were added. Results of further observations of the consortium on continuous bioremediation with the same treatment showed decontamination of chromium efficiency that reached about 94%. In addition, pH values decreased efficiency at approximately 7.3 in 14 days of incubation. The biological oxygen demand, chemical oxygen demand, and sulfate concentrations also decreased at around 89%, 92%, and 91%, respectively. SRB immobilization with zeolite-induced biofilm formation was observed at 9 days, and it further increased at 14 days. SRB cells observed were attached to the surface of the zeolite, between cells connected to each other by extracellular polymeric substances. The mass of sulfur and chromium on the surface of the zeolite increased from the 9th and 14th days. Sulfur increased from 0.07% to 0.27%, whereas chromium increased from 0.21% to 0.84%. The increase in the percentage of the two elements on the zeolite surface indicated the decontamination of sulfate and chromium pollutants in wastewater.References
Aguilar-Rivera, N. 2019. A framework for the analysis of socioeconomic and geographic sugarcane agro industry sustainability. Socio-Economic Planning Sciences 66:149-160, doi:10.1016/j.seps.2018.07.006.
Ajaz, M., Rehman, A., Khan, Z., Nisar, M.A. and Hussain, S. 2019. Degradation of azo dyes by Alcaligenes aquatilis 3c and its potential use in the wastewater treatment. AMB Express 9:64, doi:10.1186/s13568-019-0788-3.
Alimba, C.G., Dhillon, V., Bakare, A.A. and Fenech, M. 2016. Genotoxicity and cytotoxicity of chromium, copper, manganese and lead, and their mixture in WIL2-NS human B lymphoblastoid cells is enhanced by folate depletion. Mutation Research. Genetic Toxicology and Environmental Mutagenesis 798-799:35–47, doi:10.1016/j.mrgentox.2016.02.002.
Allegretta, I., Legrand, S., Alfeld, M., Gattullo, C.E., Porfido, C., Spagnuolo, M., Janssens, K. and Terzano, R. 2022. SEM-EDX hyperspectral data analysis for the study of soil aggregates. Geoderma 406:115540, doi:10.1016/j.geoderma.2021.115540.
Amala, P.V., Sumithra, T.G., Reshma, K.J., Anju, F., Subramannian, S. and Vijayagopal, P. 2020. Analytical validation of a modified turbidimetric assay to screen sulphur oxidizing bacteria. Journal of Microbiological Methods 176: 105998, doi: 10.1016/j.mimet.2020.105998.
APHA. 2017 Standard Methods for the Examination of Water and Wastewater, 23rd edition. Baird, R.B., Eaton, A.D. and Rice, E.W. (Eds). American Public Health Association, American Water Works Association, Water Environment Federation.
Banerjee, S., Misra, A., Chaudhury, S. and Dam, B. 2019. A Bacillus strain TCL isolated from Jharia coalmine with remarkable stress responses, chromium reduction capability and bioremediation potential. Journal of Hazardous Materials 367:215-223, doi:10.1016/j.jhazmat.2018.12.038.
Chaturvedi, A., Rai, B.N., Singh, R.S. and Jaiswal, R.P. 2021. Comparative toxicity assessment using plant and luminescent bacterial assays after anaerobic treatments of dyeing wastewater in a recirculating fixed bed bioreactor. Journal of Environmental Chemical Engineering 9:105466, doi:10.1016/j.jece.2021.105466.
Colin, Y., Goñi-Urriza, M., Caumette, P. and Guyoneaud, R. 2015. Contribution of enrichments and resampling for sulfate reducing bacteria diversity assessment by high-throughput cultivation. Journal of Microbiological Methods 110:92-97, doi:10.1016/j.mimet.2015.01.003.
Coutinho, C.M.L.M.C., Coutinho-Silva, R., Zinkevich, V., Pearce, C.B., Ojcius, D.M. and Beech, I. 2017. Sulphate-reducing bacteria from ulcerative colitis patients induce apoptosis of gastrointestinal epithelial cells. Microbial Pathogenesis 112:126-134, doi:10.1016/j.micpath.2017.09.054.
da Silva, S.M., Voordouw, J., Leitão, C., Martins, M., Voordouw, G. and Pereira, I.A.C. 2013. Function of formate dehydrogenases in Desulfovibrio vulgaris Hildenborough energy metabolism. Microbiology 159:1760-1769, doi:10.1099/mic.0.067868-0.
Dong, L., Zhou, S., He, Y., Jia, Y., Bai, Q., Deng, P., Gao, J., Li, Y. and Xiao, H. 2018. Analysis of the genome and chromium metabolism-related genes of Serratia sp. S2. Applied Biochemistry and Biotechnology 185:140-152, doi:10.1007/s12010-017-2639-5.
Emami Moghaddam, S.A.E., Harun, R., Mokhtar, M.N. and Zakaria, R. 2018. Potential of zeolite and algae in biomass immobilization. BioMed Research International 2018:6563196, doi:10.1155/2018/6563196.
Garrett, T.R., Bhakoo, M. and Zhang, Z. 2008. Bacterial adhesion and biofilm on surfaces. Progress in Natural Science 18:1049-1056, doi:10.1016/j.pnsc.2008.04.001.
Gong, C.J., Dan, S.U., Wang, X., Yu, P.U. and Wang, T.J. 2018. Impacts of cold-resistant mixed strains immobilized by different carrier materials on remediation of PAHs polluted soils. Chinese Journal of Ecology 37:3713-3720.
Gu, W., Zheng, D., Li, D., Wei, C., Wang, X., Yang, Q., Tian, C. and Cui, M. 2021. Integrative effect of citrate on Cr(â…¥) and total Cr removal using a sulfate-reducing bacteria consortium. Chemosphere 279:130437, doi:10.1016/j.chemosphere.2021.130437.
Huang, J., Wu, G., Zeng, R., Wang, J., Cai, R., Ho, J.C.M., Zhang, J. and Zheng, Y. 2017. Chromium contributes to human bronchial epithelial cell carcinogenesis by activating Gli2 and inhibiting autophagy. Toxicology Research 6:324-332, doi:10.1039/C6TX00372A.
Hussain, A. and Qazi, J.I. 2016. Application of sugarcane bagasse for passive anaerobic biotreatment of sulphate rich wastewaters. Applied Water Science 6:205-211.
Ihsanullah, I., Jamal, A., Ilyas, M., Zubair, M., Khan, G. and Atieh, M.A. 2020. Bioremediation of dyes: current status and prospects. Journal of Water Process Engineering 38:01680, doi:10.1016/j.jwpe.2020.101680.
Jia, Y., Zhou, M., Chen, Y., Luo, J. and Hu, Y. 2019. Carbon selection for nitrogen degradation pathway by Stenotrophomonas maltophilia: based on the balances of nitrogen, carbon and electron. Bioresource Technology 294:122114, doi:10.1016/j.biortech.2019.122114.
K.v.g, R., Argulwar, S., Sudakaran, S.V., Pulimi, M., Chandrasekaran, N. and Mukherjee, A. 2018. Nano-Bio sequential removal of hexavalent chromium using polymer-nZVI composite film and sulfate reducing bacteria under anaerobic condition. Environmental Technology and Innovation 9:122-133, doi:10.1016/j.eti.2017.11.006.
Karthik, C., Barathi, S., Pugazhendhi, A., Ramkumar, V.S., Thi, N.B.D. and Arulselvi, P.I. 2017. Evaluation of Cr(VI) reduction mechanism and removal by Cellulosimicrobium funkei strain AR8, a novel haloalkaliphilic bacterium. Journal of Hazardous Materials 333:42-53, doi:10.1016/j.jhazmat.2017.03.037.
Kiran, M.G., Pakshirajan, K. and Das, G. 2017. Heavy metal removal from multicomponent system by sulfate reducing bacteria: mechanism and cell surface characterization. Journal of Hazardous Materials 324:62-70, doi:10.1016/j.jhazmat.2015.12.042.
Kolmert, A., Wikström, P. and Hallberg, K.B. 2000. A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures. Journal of Microbiologica Methods 41(3)41:179-184, doi:10.1016/S0167-7012(00)00154-8.
Kong, Z., Wu, Z., Glick, B.R., He, S., Huang, C. and Wu, L. 2019. Co-occurrence patterns of microbial communities affected by inoculants of plant growth-promoting bacteria during phytoremediation of heavy metal-contaminated soils. Ecotoxicology and Environmental Safety 183:109504, doi:10.1016/j.ecoenv.2019.109504.
Kumar, M. and Pakshirajan, K. 2020. Novel insights into mechanism of biometal recovery from wastewater by sulfate reduction and its application in pollutant removal. Environmental Technology and Innovation 17:100542, doi:10.1016/j.eti.2019.100542.
Li, Y., Li, L. and Yu, J. 2017. Applications of zeolites in sustainable chemistry. Chem 3:928-949, doi:10.1016/j.chempr.2017.10.009.
Liu, H., Wang, Y., Zhang, H., Huang, G., Yang, Q. and Wang, Y. 2019. Synchronous detoxification and reduction treatment of tannery sludge using Cr (VI) resistant bacterial strains. Science of the Total Environment 687:34-40, doi:10.1016/j.scitotenv.2019.06.093.
Liu, X., Wu, G., Zhang, Y., Wu, D., Li, X. and Liu, P. 2015. Chromate reductase yield from Escherichia coli enhances hexavalent chromium resistance of human HepG2 cells. International Journal of Molecular Sciences 16:11892-11902, doi:10.3390/ijms160611892.
Luo, T., Huang, Z., Li, X. and Zhang, Y. 2020. Anaerobic microbe mediated arsenic reduction and redistribution in coastal wetland soil. Science of the Total Environment 727:138630, doi:10.1016/j.scitotenv.2020.138630.
Martini, C.N., Brandani, J.N., Gabrielli, M. and Vila, Mdel C. 2014. Effect of hexavalent chromium on proliferation and differentiation to adipocytes of 3T3-L1 fibroblasts. Toxicology in Vitro 28:700-706, doi:10.1016/j.tiv.2014.02.003.
Michailides, M.K., Tekerlekopoulou, A.G., Akratos, C.S., Coles, S., Pavlou, S. and Vayenas, D.V. 2015. Molasses as an efficient low-cost carbon source for biological Cr(VI) removal. Journal of Hazardous Materials 281:95-105, doi:10.1016/j.jhazmat.2014.08.004.
Minister of the Environment of the Republic of Indonesia. 2014. Regulation of the Minister of Environment of the Republic of Indonesia Number 5 of 2014 concerning Wastewater Quality Standards. Jakarta (in Indonesian).
Montalvo, S., Huiliñir, C., Gálvez, D., Roca, N. and Guerrero, L. 2016. Autotrophic denitrification with sulfide as electron donor: effect of zeolite, organic matter and temperature in batch and continuous UASB reactors. International Biodeterioration and Biodegradation 108:158-165, doi:10.1016/j.ibiod.2015.12.022.
Niu, Z.S., Yan, J., Guo, X.P., Xu, M., Sun, Y., Tou, F.Y., Yin, G.Y., Hou, L.J., Liu, M. and Yang, Y. 2021. Human activities can drive sulfate-reducing bacteria community in Chinese intertidal sediments by affecting metal distribution. Science of the Total Environment 786:147490, doi:10.1016/j.scitotenv.2021.147490.
Noviello, M., Gattullo, C.E., Faccia, M., Paradiso, V.M. and Gambacorta, G. 2021. Application of natural and synthetic zeolites in the oenological field. Food Research International 150:110737, doi:10.1016/j.foodres.2021.110737.
Peng, W., Li, X., Liu, T., Liu, Y., Ren, J., Liang, D. and Fan, W. 2018. Biostabilization of cadmium contaminated sediments using indigenous sulfate reducing bacteria: efficiency and process. Chemosphere 201:697-707, doi:10.1016/j.chemosphere.2018.02.182.
Prabhakaran, D.C., Bolaños-Benitez, V., Sivry, Y., Gelabert, A., Riotte, J. and Subramanian, S. 2019 Mechanistic studies on the bioremediation of Cr(VI) using Sphingopyxis macrogoltabida SUK2c, a Cr(VI) tolerant bacterial isolate. Biochemical Engineering Journal 150:107292, doi:10.1016/j.bej.2019.107292.
Princy, S., Sathish, S.S., Cibichakravarthy, B. and Prabagaran, S.R. 2020. Hexavalent chromium reduction by Morganella morganii (1Ab1) isolated from tannery effluent contaminated sites of Tamil Nadu, India. Biocatalysis and Agricultural Biotechnology 23:101469, doi:10.1016/j.bcab.2019.101469.
Retnaningrum, E. and Wilopo, W. 2017. Removal of sulphate and manganese on synthetic wastewater in sulphate reducing bioreactor using Indonesian natural zeolite. Indonesian Journal of Chemistry 17:203-210, doi:10.22146/ijc.22710.
Reyes-Alvarado, L.C., Okpalanze, N.N., Rene, E.R., Rustrian, E., Houbron, E., Esposito, G. and Lens, P.N.L. 2017. Carbohydrate based polymeric materials as slow release electron donors for sulphate removal from wastewater. Journal of Environmental Management 200:407-415, doi:10.1016/j.jenvman.2017.05.074.
Rezaei, M. and Mehrnia, M.R. 2014 The influence of zeolite (clinoptilolite) on the performance of a hybrid membrane bioreactor. Bioresource Technology 158:25-31, doi:10.1016/j.biortech.2014.01.138.
Rezvantala, S. and Bahadori, F. 2015. Application of natural zeolites on wastewater treatment. Asian Journal of Agricultural Research 9:343-349, doi:10.3923/ajar.2015.343.349.
Roy-Basu, A., Bharat, G.K., Chakraborty, P. and Sarkar, S.K. 2020. Adaptive co-mnagement model for the East Kolkata wetlands: a sustainable solution to manage the rapid ecological transformation of a peri-urban landscape. Science of the Total Environment 698:134203, doi:10.1016/j.scitotenv.2019.134203.
Sahinkaya, E., Yurtsever, A., Isler, E., Coban, I. and Aktaş, Ö. 2018. Sulfate reduction and filtration performances of an anaerobic membrane bioreactor (AnMBR). Chemical Engineering Journal 349:47-55, doi:10.1016/j.cej.2018.05.001.
Shiping, S., Zhaohui, G., Ping, L., Yushuang, W., Yilu, L., Wei, C., Min, Z., Shandong, W. and Hongwei, Y. 2018. Simultaneous mitigation of tissue cadmium and lead accumulation in rice via sulfate-reducing bacterium. Ecotoxicology and Environmental Safety 169:292-300, doi:10.1016/j.ecoenv.2018.11.030.
Takahashi, C., Ueno, K., Aoyama, J., Adachi, M. and Yamamoto, H. 2017. Imaging of intracellular behavior of polymeric nanoparticles in Staphylococcus epidermidis bio fi lms by slit-scanning confocal Raman microscopy and scanning electron microscopy with energy-dispersive X-ray spectroscopy. Materials Science and Engineering. C, Materials for Biological Applications 76:1066-1074, doi:10.1016/j.msec.2017.03.132.
Tan, H., Wang, C., Zeng, G., Luo, Y., Li, H. and Xu, H. 2020. Bioreduction and biosorption of Cr(VI) by a novel Bacillus sp. CRB-B1 strain. Journal of Hazardous Materials 386:121628, doi:10.1016/j.jhazmat.2019.121628.
Valdés, M.G., Pérez-Cordoves, A.I. and DÃaz-GarcÃa, M.E. 2006 Zeolites and zeolite-based materials in analytical chemistry. TrAC Trends in Analytical Chemistry 25:24-30, doi:10.1016/j.trac.2005.04.016.
Verma, R., Sharma, S., Kundu, L.M. and Pandey, L.M. 2020. Experimental investigation of molasses as a sole nutrient for the production of an alternative metabolite biosurfactant. Journal of Water Process Engineering 38:101632, doi:10.1016/j.jwpe.2020.101632.
Wang, Y., Chai, L., Liao, Q., Tang, C., Liao, Y., Peng, B. and Yang, Z. 2016. Structural and genetic diversity of hexavalent chromium-resistant bacteria in contaminated soil. Geomicrobiology Journal 33:222-229, doi:10.1080/01490451.2015.1054006.
Wang, Z., Chen, X. and Zhao, H.P. 2022. Model-based analyses of chromate, selenate and sulfate reduction in a methane-based membrane biofilm reactor. Environment International 158:106925, doi:10.1016/j.envint.2021.106925.
Yacout, D.M.M. and Hassouna, M.S. 2016. Identifying potential environmental impacts of waste handling strategies in textile industry. Environmental Monitoring and Assessment 188:445, doi:10.1007/s10661-016-5443-8.
Yan, J., Ye, W., Jian, Z., Xie, J., Zhong, K., Wang, S., Hu, H., Chen, Z., Wen, H. and Zhang, H. 2018. Enhanced sulfate and metal removal by reduced graphene oxide self-assembled Enterococcus avium sulfate-reducing bacteria particles. Bioresource Technology 266: 447-453, doi:10.1016/j.biortech.2018.07.012.
Yang, Q., Han, B., Xue, J., Lv, Y., Li, S., Liu, Y., Wu, P., Wang, X. and Zhang, Z. 2020. Hexavalent chromium induces mitochondrial dynamics disorder in rat liver by inhibiting AMPK/PGC-1α signaling pathway. Environmental Pollution 265:114855, doi:10.1016/j.envpol.2020.114855.
Yang, X., Liu, P., Yao, M., Sun, H., Liu, R., Xie, J. and Zhao, Y. 2021. Mechanism and enhancement of Cr(VI) contaminated groundwater remediation by molasses. Science of the Total Environment 780:146580, doi:10.1016/j.scitotenv.2021.146580.
Zan, F., Liang, Z., Jiang, F., Dai, J. and Chen, G. 2019. Effects of food waste addition on biofilm formation and sulfide production in a gravity sewer. Water Research 157:74-82.
Zeng, Q., Hao, T., Mackey, H.R., Wei, L., Guo, G. and Chen, G. 2017. Alkaline textile wastewater biotreatment: a sulfate-reducing granular sludge based lab-scale study. Journal of Hazardous Materials 332:104-111, doi:10.1016/j.jhazmat.2017.03.005.
Zeng, Q., Wang, Y., Zan, F., Khanal, S.K. and Hao, T. 2021. Biogenic sulfide for azo dye decolorization from textile dyeing wastewater. Chemosphere 283:131158, doi:10.1016/j.chemosphere.2021.131158.
Zhang, M., Wang, H. and Han, X. 2016. Preparation of metal-resistant immobilized sulfate reducing bacteria beads for acid mine drainage treatment. Chemosphere 154:215-223, doi:10.1016/j.chemosphere.2016.03.103.
Zhou, C., Zhou, Y. and Rittmann, B.E. 2017. Reductive precipitation of sulfate and soluble Fe(III) by Desulfovibrio vulgaris: electron donor regulates intracellular electron flow and Nano-FeS crystallization. Water Research 119:91-101, doi:10.1016/j.watres.2017.04.044.
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