Abstract
Bioremediation of Cr(VI) by microorganisms has attracted immense research interests. There are three different mechanisms for bioremediation of Cr(VI): biosorption, bioreduction, and biomineralization. Identifying the relative contributions of these different mechanisms to Cr(VI) bioremediation can provide valuable information to enhance the final result. This article explores the corresponding contributions of different mechanisms in the Cr(VI) bioremediation process. To obtain a deeper understanding of each bioremediation mechanism, the corresponding precipitation products were analyzed via different methods. Fourier transform infrared spectrometer (FTIR) analysis showed that Cr(VI) was adsorbed by functional groups in EPS to form a chelate compound. X-ray photoelectron spectroscopy (XPS) and X-ray diffraction (XRD) analysis determined that the stable Cr(III) compounds and mineral crystals which contain chromium gradually formed during the bioremediation process. High-throughput sequencing technology was applied to monitor microbial community succession. The results showed that the total removal rate of Cr(VI) reached 77.64% in 56 days in 100 mg/L Cr(VI). Bioreduction was the major contributor to the final result, followed by biosorption and biomineralization; their proportions are 69.61%, 19.16%, and 11.23%, respectively. Besides, the high-throughput sequencing data indicated that reductive microorganisms were the dominant flora and that the relative abundance of different reductive microorganism types changes significantly. This work has clarified the contributions of different mechanisms during Cr(VI) bioremediation process and provided a new enhancement strategy for Cr(VI) bioremediation.
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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Agarwal A, Singh HP, Rai JPN (2014) Chromium phytoextraction from tannery effluent-contaminated soil by Crotalaria juncea infested with Pseudomonas fluorescens. Environ Sci Pollut R 21(13):7938–7944
Bai J, Xun P, Morris S, Jacobs DRJ, Liu K, He K (2015) Chromium exposure and incidence of metabolic syndrome among American young adults over a 23-year follow-up: the CARDIA Trace Element Study. Sci Rep 5:15606–15613
Balaz M, Bujnakova Z, Achimovicova M (2019) Simultaneous valorization of polyvinyl chloride and eggshell wastes by a semi-industrial mechanochemical approach. Environ Res 170:332–336
Banerjee S, Misra A, Chaudhury S, Dam BB (2019) A Bacillus strain TCL isolated from Jharia coalmine with remarkable stress responses, chromium reduction capability and bioremediation potential. J Hazard Mater 367:215–223
Bhattaraia DP, Awasthi GP, Maharjana B, Lee J, Kim BS, Park HC, Kim CS (2019) Synthesis of polythiophene nanoparticles by surfactant-free chemical oxidative polymerization method: characterization, in vitro biomineralization, and cytotoxicity evaluation. J Ind And Eng Chem 77:243–252
Chen JM, Hao OJ (1996) Environmental factors and modeling in microbial chromium(VI) reduction. Water Envioron Res 68(7):1165–1164
Chen GJ, Bai YA, Zeng JX, Qin LP (2019) Effects of different metabolic pathways and environmental parameters on Cr isotope fractionation during Cr(VI) reduction by extremely thermophilic bacteria. Geochimica et Cosmochinica Acta 256:135–146
Chug R, Gour VS, Mathur S, Kothari SL (2016) Optimization of extracellular polymeric substances production using Azotobacter beijreinckii and Bacillus subtilis and its application in chromium(VI) removal. Bioresour Technol 214:604–608
Cummings DE, Fendorf S, Singh S (2007) Reduction of Cr(VI) under acidic conditions by the facultative Fe(III)-reducing bacterium Acidiphilium cryptum. Environ Sci Technol 41(1):146–152
Dai W, Fang Y, Yu L, Zhao G, Yan X (2018) Rubidium ion capture with composite adsorbent PMA@HKUST-1. J Taiwan Inst Chem Eng 84:222–228
Das S, Mishra J, Das SK, Pandey S, Rao DS, Chakraborty A (2014) Investigation on mechanism of Cr(VI) reduction and removal by Bacillus amyloliquefaciens, a novel chromate tolerant bacterium isolated from chromite mine soil. Chemosphere 96:112–121
Durán U, Coronado-Apodaca KG, Meza-Escalante ER, Ulloa-Mercado G, Serrano D (2018) Two combined mechanisms responsible to hexavalent chromium removal on active anaerobic granular consortium. Chemosphere 198:191–197
Fernández PM, Viñarta SC, Bernal AR (2018) Bioremediation strategies for chromium removal: current research, scale-up approach and future perspectives. Chemosphere 208:139–148
Florentino AP, Jan WM, Stams AJM, Amdrea IS (2015) Sulfur reduction in acid rock drainage environments. Environ Sci Technol 49:11746–11755
Gopal B, Gupta A (2019) Integrated Approach for Hazardous Cr(VI) Removal: reduction, extraction, and conversion into a photoactive composite, CuO/ CuCr2O4. ACS Omega 4:20443–20449
Guo H, Nasir M, Lv JL, Dai YC, Gao JK (2017) Understanding the variation of microbial community in heavy metals contaminated soil using high throughput sequencing. Ecotox Environ Safe 144:300–306
He T, Zhang YZ, Kong XJ, Yu J, Lv XL, Wu Y, Guo Z, Li JR (2018) Zr(IV)-Based metal organic framework with T shaped ligand: unique structure, high stability, selective detection, and rapid adsorption of Cr2O72- in water. ACS Appl Mater Interfaces 10:16650–16659
Huang H, Wu K, Khan A, Jiang Y, Ling Z, Liu P (2016) A novel Pseudomonas gessardii strain LZ-E simultaneously degrades naphthalene and reduces hexavalent chromium. Bioresour Technol 207:370–378
Huang XN, Min D, Liu DF, Cheng L, Qian C, Li WW, Yu HQ (2019) Formation mechanism of organo-chromium (III) complexes from bioreduction of chromium(VI) by Aeromonas hydrophila. Environ Int 129:86–94
Ishak AF, Karim AN, Ahmad WA, Zakaria ZA (2016) Chromate detoxification using combination of chromeBac system and immobilized chromate reductase beads. Int Biodeter Bioegr 113:238–243
Jobby R, Jha P, Yadav AK (2018) Biosorption and biotransformation of hexavalent chromium [Cr(VI)]: a comprehensive review. Chemosphere 207:255–266
Khalifa GM, Kirchenbuechler D, Koifman N, Kleinerman O, Talmon Y, Elbaum M (2016) Biomineralization pathways in a foraminifer revealed using a novel correlative cryo-fluorescence-SEM-EDS technique. J Struct Biol 196(2):155–163
Li B, Pan D, Zheng J (2008) Microscopic investigations of the Cr(VI) uptake mechanism of living, Ochrobactrum anthropic. Langmuir 24(17):9630–9635
Li F, Wang W, Li CC, Zhu RL, Ge F (2018b) Self-mediated pH changes in culture medium affecting biosorption and biomineralization of Cd 2+, by Bacillus cereus Cd01. J Hazard Mater 358:178–186
Li MK, He ZG, Hu YT, Hu L, Zhong H (2019) Both cell envelope and cytoplasm were the locations for chromium(VI) reduction by Bacillus sp. M6. Bioresour Technol 273:130–135
Li SG, Chen WW, Zhan AB, Liang J (2018a) Identification and characterization of microRNAs involved in scale biomineralization in the naked carp Gymnocypris przewalskii. Comp Biochem Phys D 28:196–203
Li XL, Ding CC, Liao JL, Du L, Liu N, Sun Q (2016) Microbial reduction of Uranium(VI) by Bacillus sp. dwc-2: a macroscopic and spectroscopic study. J Environ Sci 53(3):9–15
Liu B, Su GR, Yang YR, Yao Y, Huang YJ, Zhong H, He ZG (2019a) Vertical distribution of microbial communities in chromium-contaminated soil and isolation of Cr(VI)-Reducing strains. Ecotox Environ Safe 180:242–251
Liu T, Wang Y, Pan S, Zhang QY (2019b) The addition of copper accelerates the corrosion of steel via impeding biomineralized film formation of Bacillus subtilis in seawater. Corrosion Ence 149:153–163
Luo QL, Chen Z, Li YX, Wang YM, Cai LF, Wang LY, Liu SR, Wang ZZ, Peng YJ, Wang YP (2019) Highly efficient and recyclable Shewanella xiamenensis-grafted graphene oxide/poly(vinyl alcohol) biofilm catalysts for increased Cr(VI) reduction. ACS Sustain Chem Eng 7:12611–12620
Ma LL, Xu JM, Chen N, Li M, Feng C (2019a) Microbial reduction fate of chromium (Cr) in aqueous solution by mixed bacterial consortium. Ecotox Environ Safe 170:763–770
Ma Y, Zhong H, He ZG (2019b) Cr(VI) reductase activity locates in the cytoplasm of Aeribacillus pallidus BK1, a novel Cr(VI)-reducing thermophile isolated from Tengchong geothermal region. China Chem Eng J 371:524–534
Mambrey V, Rakete S, Tobollikd M, Shoko D, Moyog D, Schutzmeier P, Steckling-Muschackc N, Muteti-Fana S, Bose-O’Reilly S (2020) Artisanal and small-scale gold mining: a cross-sectional assessment of occupational mercury exposure and exposure risk factors in Kadoma and Shurugwi, Zimbabwe. Environ Res 184:109379–109396
Mody BR, Bindra MO, Modi VV (1989) Extracellular polysaccharides of cowpea rhizobia: compositional and functional studies. Arch Microbiol 1:2–5
Pavithra KG, Jaikumar V, Kumar SP, Rajan PS (2019) A review on cleaner strategies for chromium industrial wastewater: present research and future perspective. J Clean Prod 228:580–593
Pradhan D, Sukla LB, Mishra BB (2018) Biosorption for removal of hexavalent chromium using microalgae Scenedesmus sp. J Clean Prod 209:617–629
Rambabua K, Bharatha G, Banata F, Show PL (2020) Biosorption performance of date palm empty fruit bunch wastes for toxic hexavalent chromium removal. Environ Res 187:109694–109709
Ren YM, Mei L, Gu YC, Zhao N, Wang YL, Guo G (2019) Stereocomplex crystallite-based eco-friendly nanofiber membranes for removal of Cr(VI) and antibacterial effects. ACS Sustain Chem Eng 7:16072–16083
Rizvi A, Ahmed B, Zaidi A, Khan MS (2019) Bioreduction of toxicity influenced by bioactive molecules secreted under metal stress by Azotobacter chroococcum. Ecotoxicology 28:302–322
Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: a review. Chemosphere 178:513–533
Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11(3):229–254
Singh R, Kumar A, Kirrolia A, Kumar R, Yadav N, Bishnoi NR (2011) Removal of sulphate, Cod and Cr(VI) in simulated and real wastewater by sulphate reducing bacteria enrichment in small bioreactor and FTIR study. Bioresour Technol 102(2):677–682
Su JF, Shi JX, Huang TL, Ma F (2016) Kinetic analysis of simultaneous denitrification and biomineralization of novel Acinetobacter sp. CN86. Mar Pollut Bull 109(1):87–94
Thatoi H, Das S, Mishra J, Ratha BP, Das N (2014) Bacterial chromate reductase, a potential enzyme for bioremediation of hexavalent chromium: A review. J Environ Manage 146(15):383–399
Tu H, Yuan G, Zhao C, Liu J, Li F, Yang J (2019) U-phosphate biomineralization induced by Bacillus sp. dw-2 in the presence of organic acids. Nucl Eng Technol 51:1–14
Wang J, Li Q, Li MM, Chen TH, Zhou YF, Yue ZB (2014) Competitive adsorption of heavy metal by extracellular polymeric substances (EPS) extracted from sulfate reducing bacteria. Bioresour Technol 163:374–376
Wang XL, Li Y, Huang J, Zhou YZ, Li BL, Liu DB (2019) Efficiency and mechanism of adsorption of low concentration uranium in water by extracellular polymeric substances. J Environ Radioact 197:81–89
Wu M, Li Y, Li J, Wang Y, Xu H, Zhao Y (2019) Bioreduction of hexavalent chromium using a novel strain CRB-7 immobilized on multiple materials. J Hazard Mater 368:412–420
Xie Y, Fang ZB, Li L, Yang HX, Liu TF (2019) Creating chemisorption sites for enhanced CO2 photoreduction activity through alkylamine modification of MIL-101-Cr. ACS Appl Mater 11(30):27017–27023
Ye B, Luo Y, He J, Sun L, Long B, Liu Q (2018) Investigation of lead bioimmobilization and transformation by Penicillium oxalicum SL2. Bioresour Technol 3:206–210
Ye Z, Yin X, Chen L, He X, Lin Z, Liu C, Ning S, Wang X, Wei Y (2019) An integrated process for removal and recovery of Cr(VI) from electroplating wastewater by ion exchange and reduction–precipitation based on a silica-supported pyridine resin. J Clean Prod 236:117631–117639
Yin K, Wang QN, Lv M, Chen LX (2019) Microorganism remediation strategies towards heavy metals. Chem Eng J 360:1553–1563
Yue ZB, Li Q, Li CC, Chen TH, Wang J (2015) Component analysis and heavy metal adsorption ability of extracellular polymeric substances (EPS) from sulfate reducing bacteria. Bioresour Technol 194:399–402
Zhang JK, Wang ZH, Ye Y (2016) Heavy metal resistances and chromium removal of a novel Cr(VI)-reducing Pseudomonad strain isolated from circulating cooling water of iron and steel plant[J]. Appl Biochem Biotechnol 180(7):1328–1344
Zhang J, Song H, Chen Z (2018) Biomineralization mechanism of U(VI) induced by, Bacillus cereus, 12-2: the role of functional groups and enzymes. Chemosphere 206:682–692
Zhu Y, Li H, Zhang GX, Meng FJ, Li LF, Wu S (2018) Removal of hexavalent chromium from aqueous solution by different surface-modified biochars: acid washing, nanoscale zero-valent iron and ferric iron loading. Bioresour Technol 261:142–150
Zhu YF, Yan JW, Xia L, Zhang X, Luo LX (2019) mechanisms of Cr(VI) reduction by Bicallus sp.CRB-1, a novel Cr(VI)-reducing bacterium isolated from tannery activated sludge. Ecotox Environ Safe 186:109792–109799
Acknowledgments
We thank National Engineering Laboratory of Biohydrometallurgy, GRINM Group Corporation Limited, China, for their support during the experiments.
Funding
This work was supported by the National Natural Science Foundation of China (51974279, U1402234 and 41573074); National Key Research and Development Project of China (2018YFC1802702, 2018YFC1801803, 2019YFC1805903).
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Xiao Yan, Xingyu Liu, Mingjiang Zhang, Jianlei Wang, and Xuewu Hu. The first draft of the manuscript was written by Xiao Yan and Jianlei Wang and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Highlights
• 77.64% removal rate of Cr(VI) was achieved by the reductive microbes (Stenotrophomonas maltophilia, Ochrobactrum sp., Bacillus megaterium strain, and Pseudomonas putida).
• The contribution of biosorption, bioreduction, and biomineralization in the total removal rate of Cr(VI) was calculated; the main contributor was bioreduction, followed by biosorption and biomineralization, accounting for 69.61, 19.16, and 11.23%, respectively.
• The FTIR, XPS, XRD, and TEM-EDS analysis of precipitation products confirmed the corresponding bioremediation mechanisms.
• VThe microbial community succession indicated that the relative abundance of different microbial species changed greatly, but the reductive microbial species was still dominant microorganisms, suggesting the reductive microbial species were more stable during the bioremediation process.
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Yan, X., Liu, X., Zhang, M. et al. Lab-scale evaluation of the microbial bioremediation of Cr(VI): contributions of biosorption, bioreduction, and biomineralization. Environ Sci Pollut Res 28, 22359–22371 (2021). https://doi.org/10.1007/s11356-020-11852-3
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DOI: https://doi.org/10.1007/s11356-020-11852-3