Abstract
This study constructed an up-flow anaerobic column reactor fed with synthetic sulfate-rich cadmium (Cd(II))-bearing wastewater, for investigating its Cd(II) removal performance and mechanism. Long-term experiment results manifest that introducing Cd(II) into influent led to an enhanced sulfate removal but did not increase the effluent sulfide concentration, implying the CdS formation. When influent Cd(II) concentration was shifted from 50 to 100 mg/L, the median Cd(II) removal rate was increased from 13.6 to 32.2 mg/(L·d). Batch tests indicate that the uptake and sequestration function of anaerobes merely led to a small portion of Cd(II) removal. A majority of aqueous Cd(II) (86.3%) was eliminated by precipitation reactions. The generated precipitates were found to be dominantly presented in carbonate, Fe–Mn oxide, sulfide bound and residue forms, which account for 92.6–93.9% of total Cd content of sludge obtained at diverse operation phases. The crystallographic CdS (i.e., residue fraction) particles have nano-scale sizes, and the relatively high atomic ratio of S to Cd was likely due to the adsorption/deposition of other sulfides. The dominant sulfate-reducing bacteria (SRB) were recognized as Desulfurella, Desulforhabdus and Desulfovibrio, and the primary competitor with them for substrate utilization were identified to be methanogens.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All relevant data are included in the paper or its Supplementary Information.
References
APHA (1995) Standard methods for examination of water and wastewater, 19th edn. American Public Health Association Inc., New York
Awual MR (2019) A facile composite material for enhanced cadmium(II) ion capturing from wastewater. J Environ Chem Eng 7(5):103378. https://doi.org/10.1016/j.jece.2019.103378
Ayangbenro AS, Olanrewaju OS, Babalola OO (2018) Sulfate-reducing bacteria as an effective tool for sustainable acid mine bioremediation. Front Microbiol 9:1986. https://doi.org/10.3389/fmicb.2018.01986
Bai HJ, Zhang ZM, Guo Y, Yang GE (2009) Biosynthesis of cadmium sulfide nanoparticles by photosynthetic bacteria Rhodopseudomonas palustris. Colloids Surf B 70(1):142–146. https://doi.org/10.1016/j.colsurfb.2008.12.025
Bakhshi M, Hosseini MR (2016) Synthesis of CdS nanoparticles from cadmium sulfate solutions using the extracellular polymeric substances of B. licheniformis as stabilizing agent. Enzyme Microb Technol 95:209–216. https://doi.org/10.1016/j.enzmictec.2016.08.011
Baloch MI, Akunna JC, Kierans M, Collier PJ (2008) Structural analysis of anaerobic granules in a phase separated reactor by electron microscopy. Bioresour Technol 99(5):922–929. https://doi.org/10.1016/j.biortech.2007.03.016
Byun IG, Lee TH, Kim YO, Song SK, Park TJ (2004) Activity of sulphate reducing bacteria according to COD/SO42- ratio of acrylonitrile wastewater containing high sulphate. Water Sci Technol 49:229–235. https://doi.org/10.2166/wst.2004.0758
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Carolin CF, Kumar P, Saravanan A, Joshiba GJ, Naushad M (2017) Efficient techniques for the removal of toxic heavy metals from aquatic environment: a review. J Environ Chem Eng 5(3):2782–2799. https://doi.org/10.1016/j.jece.2017.05.029
Chen J, Deng S, Jia W, Li X, Chang J (2021) Removal of multiple heavy metals from mining-impacted water by biochar-filled constructed wetlands: adsorption and biotic removal routes. Bioresour Technol 331:125061. https://doi.org/10.1016/j.biortech.2021.125061
Chen Y, Qian H, Wu F, Zhou J (2011) Clearance and recovery of Cd(II) from aqueous solution by magnetic separation technology. Chemosphere 83(9):1214–1219. https://doi.org/10.1016/j.chemosphere.2011.03.043
de Godoi LAG, dos Santos CED, Foresti E, Damianovic MHRZ (2017) Evaluating and refining alkalinity calculations due to sulfide and bicarbonate accessed by titration in anaerobic sulfate-reducing bioreactors. Water Air Soil Pollut 228:322. https://doi.org/10.1007/s11270-017-3518-y
de Matos LP, Costa PF, Moreira M, Gomes PCS, Silva SD, Gurgel LVA, Teixeira MC (2018) Simultaneous removal of sulfate and arsenic using immobilized non-traditional SRB mixed culture and alternative low-cost carbon sources. Chem Eng J 334:1630–1641. https://doi.org/10.1016/j.cej.2017.11.035
Gallegos-Garcia M, Celis LB, Rangel-Méndez R, Razo-Flores E (2009) Precipitation and recovery of metal sulfides from metal containing acidic wastewater in a sulfidogenic down-flow fluidized bed reactor. Biotechnol and Bioeng 102(1):91–99. https://doi.org/10.1002/bit.22049
Gam ZB, Thioye A, Cayol JL, Joseph M, Fauque G, Labat M (2018) Characterization of Desulfovibrio salinus sp. nov., a slightly halophilic sulfate-reducing bacterium isolated from a saline lake in Tunisia. Int J Syst Evol Microbiol 68(3):715–720. https://doi.org/10.1099/ijsem.0.002567
Giordani A, Rodriguez RP, Sancinetti GP, Hayashi EA, Beli E, Brucha G (2019) Effect of low pH and metal content on microbial community structure in an anaerobic sequencing batch reactor treating acid mine drainage. Miner Eng 141:105860. https://doi.org/10.1016/j.mineng.2019.105860
Gonzalez-Silva BM, Briones-Gallardo R, Razo-Flores E, Celis LB (2009) Inhibition of sulfate reduction by iron, cadmium and sulfide in granular sludge. J Hazard Mater 172(1):400–407. https://doi.org/10.1016/j.jhazmat.2009.07.022
Han X, Wang Z, Zhu C, Wu Z (2013) Effect of ultrasonic power density on extracting loosely bound and tightly bound extracellular polymeric substances. Desalination 329:35–40. https://doi.org/10.1016/j.desal.2013.09.002
Hao T, Xiang P, Mackey HR, Chi K, Lu H, Chui H, van Loosdrecht MCM, Chen G-H (2014) A review of biological sulfate conversions in wastewater treatment. Water Res 65:1–21. https://doi.org/10.1016/j.watres.2014.06.043
He Z-W, Tang C-C, Liu W-Z, Ren Y-X, Guo Z-C, Zhou A-J, Wang L, Wang C-X, Wang A-J (2019) Enhanced short-chain fatty acids production from waste activated sludge with alkaline followed by potassium ferrate treatment. Bioresour Technol 289:121642. https://doi.org/10.1016/j.biortech.2019.121642
Hudaib B (2021) Treatment of real industrial wastewater with high sulfate concentrations using modified Jordanian kaolin sorbent: batch and modelling studies. Heliyon 7(11):e08351. https://doi.org/10.1016/j.heliyon.2021.e08351
Jeanette B, Kristian KB, Waleed AA-S, Peter EH, Lars HH, Søren JS, Ole N (2012) Selection for Cu-tolerant bacterial communities with altered composition, but unaltered richness, via long-term Cu exposure. Appl Environ Microb 78(20):7438–7446. https://doi.org/10.1128/AEM.01071-12
Jena J, Pradhan N, Aishvarya V, Nayak RR, Dash BP, Sukla LB, Panda PK, Mishra BK (2015) Biological sequestration and retention of cadmium as CdS nanoparticles by the microalga Scenedesmus-24. J Appl Phycol 27(6):2251–2260. https://doi.org/10.1007/s10811-014-0499-8
Jiang Y, Li H, Qin Y, Liang Y, Wu C, Liu K, Yu F, Wei Q (2019) Spatial separation and bio-chain cooperation between sulfidogenesis and methanogenesis in an anaerobic baffled reactor with sucrose as the carbon source. Int Biodeterior Biodegradation 138:99–105. https://doi.org/10.1016/j.ibiod.2019.01.004
Jiménez-Rodríguez AM, Durán-Barrantes MM, Borja R, Sánchez E, Colmenarejo MF, Raposo F (2009) Heavy metals removal from acid mine drainage water using biogenic hydrogen sulphide and effluent from anaerobic treatment: Effect of pH. J Hazard Mater 165(1–3):759–765. https://doi.org/10.1016/j.jhazmat.2008.10.053
Johnson DB, Hallberg KB (2005) Biogeochemistry of the compost bioreactor components of a composite acid mine drainage passive remediation system. Sci Total Environ 338(1–2):81–93. https://doi.org/10.1016/j.scitotenv.2004.09.008
Kumar R, Rani M, Gupta H, Gupta B (2014) Trace metal fractionation in water and sediments of an urban river stretch. Chem Speciat Bioavailab 26(4):200–209. https://doi.org/10.3184/095422914X14142369069568
Kushkevych I, Dordevic D, Vitezova M (2019) Toxicity of hydrogen sulfide toward sulfate-reducing bacteria Desulfovibrio piger Vib-7. Arch Microbiol 201(3):389–397. https://doi.org/10.3184/095422914X14142369069568
Li X, Wu Y, Zhang C, Liu Y, Zeng G, Tang X, Dai L, Lan S (2016) Immobilizing of heavy metals in sediments contaminated by nonferrous metals smelting plant sewage with sulfate reducing bacteria and micro zero valent iron. Chem Eng J 306(15):393–400. https://doi.org/10.1016/j.cej.2016.07.079
Liu Y, Tie B, Li Y, Lei M, Wei X, Liu X, Du H (2018) Inoculation of soil with cadmium-resistant bacterium Delftia sp. B9 reduces cadmium accumulation in rice (Oryza sativa L.) grains. Ecotoxicol Environ Saf 163(15):223–229. https://doi.org/10.1016/j.ecoenv.2018.07.081
Loreto CD, Monge O, Martin AR, Ochoa-Herrera V, Sierra-Alvarez R, Almendariz FJ (2021) Effect of carbon source and metal toxicity for potential acid mine drainage (AMD) treatment with an anaerobic sludge using sulfate-reduction. Water Sci Technol. https://doi.org/10.2166/wst.2021.163
Martins M, Faleiro ML, Barros RJ, Veríssimo AR, Barreiros MA, Costa MC (2009) Characterization and activity studies of highly heavy metal resistant sulphate-reducing bacteria to be used in acid mine drainage decontamination. J Hazard Mater 166(2–3):706–713. https://doi.org/10.1016/j.jhazmat.2008.11.088
Medírcio SN, Leão VA, Teixeira MC (2007) Specific growth rate of sulfate reducing bacteria in the presence of manganese and cadmium. J Hazard Mater 143(1–2):593–596. https://doi.org/10.1016/j.jhazmat.2006.09.079
Mohan BS, Hosetti BB (1997) Potential phytotoxicity of lead and cadmium to lemna minor grown in sewage stabilization ponds. Environ Pollut 98(2):233–238. https://doi.org/10.1016/S0269-7491(97)00125-5
Narayan KD, Pandey SK, Das SK (2010) Characterization of Comamonas thiooxidans sp. nov., and comparison of thiosulfate oxidation with Comamonas testosteroni and Comamonas composti. Curr Microbiol 61(4):248–253. https://doi.org/10.1007/s00284-010-9602-9
Nogueira EW, de Godoi LAG, Yabuki LNM, Brucha G, Damianovic MHRZ (2021) Sulfate and metal removal from acid mine drainage using sugarcane vinasse as electron donor: Performance and microbial community of the down-flow structured-bed bioreactor. Bioresour Technol 330:124968. https://doi.org/10.1016/j.biortech.2021.124968
Nogueira EW, Licona FM, de Godoi LAG, Brucha G, Damianovic MHRZ (2019) Biological treatment removal of rare earth elements and yttrium (REY) and metals from actual acid mine drainage. Water Sci Technol 80:1485–1493. https://doi.org/10.2166/wst.2019.398
Patidar SK, Tare V (2005) Effect of molybdate on methanogenic and sulfidogenic activity of biomass. Bioresour Technol 96:1215–1222. https://doi.org/10.1016/j.biortech.2004.11.001
Paul S, Shakya AK, Ghosh PK (2020) Bacterially-assisted recovery of cadmium and nickel as their metal sulfide nanoparticles from spent Ni–Cd battery via hydrometallurgical route. J Environ Manage 261(1):110113. https://doi.org/10.1016/j.jenvman.2020.110113
Peng W, Li X, Liu T, Ren J (2018) Biostabilization of cadmium contaminated sediments using indigenous sulfate reducing bacteria: efficiency and process. Chemosphere 201:697–707. https://doi.org/10.1016/j.chemosphere.2018.02.182
Pruden A, Messner N, Pereyra L, Hanson RE, Hiibel SR, Reardon KF (2007) The effect of inoculum on the performance of sulfate-reducing columns treating heavy metal contaminated water. Water Res 41:904–914. https://doi.org/10.1016/j.watres.2006.11.025
Qi P, Zhang D, Zeng Y, Wan Y (2016) Biosynthesis of CdS nanoparticles: a fluorescent sensor for sulfate-reducing bacteria detection. Talanta 147:142–146. https://doi.org/10.1016/j.talanta.2015.09.046
Rodrigues C, Núñez-Gómez D, Follmann HVDM, Silveira DD, Nagel-Hassemer ME, Lapolli FR, Lobo-Recio MÁ (2020) Biostimulation of sulfate-reducing bacteria and metallic ions removal from coal mine-impacted water (MIW) using shrimp shell as treatment agent. J Hazard Mater 398(5):122893. https://doi.org/10.1016/j.jhazmat.2020.122893
Rzeczycka M, Miernik A, Markiewicz Z (2010) Simultaneous degradation of waste phosphogypsum and liquid manure from industrial pig farm by a mixed community of sulfate reducing bacteria. Pol J Microbiol 59:241–247
Sankhla A, Sharma R, Yadav RS, Kashyap D, Kothari SL, Kachhwaha S (2016) Biosynthesis and characterization of cadmium sulfide nanoparticles-An emphasis of zeta potential behavior due to capping. Mater Chem Phys 170:44–51. https://doi.org/10.1016/j.matchemphys.2015.12.017
Smith KS, Ingram-Smith C (2007) Methanosaeta, the forgotten methanogen? Trends Microbiol 15(5):150–155. https://doi.org/10.1016/j.tim.2007.02.002
Stams AJM, Plugge CM, de Bok FAM, van Houten BHGW, Lens P, Dijkman H, Weijma J (2005) Metabolic interactions in methanogenic and sulfate-reducing bioreactors. Water Sci Technol 52(1–2):13–20. https://doi.org/10.2166/wst.2005.0493
Tan W, Liu F, Feng X, Huang Q, Li X (2005) Adsorption and redox reactions of heavy metals on Fe–Mn nodules from Chinese soils. J Colloid Interface Sci 284(2):600–605. https://doi.org/10.1016/j.jcis.2004.10.049
Tanaka S, Lee Y-H (1997) Control of sulfate reduction by molybdate in anaerobic digestion. War Sci Tech 36(12):143–150. https://doi.org/10.1016/S0273-1223(97)00714-2
Tessier A, Campbell PGC, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51(7):844–851. https://doi.org/10.1021/ac50043a017
Thabet OB, Wafa T, Eltaief K, Cayol JL, Hamdi M, Fauque G, Fardeau ML (2011) Desulfovibrio legallis sp. nov.: a moderately halophilic, sulfate-reducing bacterium isolated from a wastewater digestor in Tunisia. Curr Microbiol 62(2):486–491. https://doi.org/10.1007/s00284-010-9733-z
van Houten BHGW, Roest K, Tzeneva VA, Dijkman H, Smidt H, Stams AJM (2006) Occurrence of methanogenesis during start-up of a full-scale synthesis gas-fed reactor treating sulfate and metal-rich wastewater. Water Res 40:553–560. https://doi.org/10.1016/j.watres.2005.12.004
Wang B, Wu D, Dai J, Ekama GA, Hao X, Chen G-H (2019) Elucidating the effects of starvation and reactivation on anaerobic sulfidogenic granular sludge: reactor performance and granular sludge transformation. Water Res 151:44–53. https://doi.org/10.1016/j.watres.2018.12.008
Wang X, Hu K, Xu Q, Lu L, Liao S, Wang G (2020) Immobilization of Cd using mixed Enterobacter and Comamonas bacterial reagents in pot experiments with Brassica rapa L. Environ Sci Technol 54(24):15731–15741. https://doi.org/10.1021/acs.est.0c03114
Wei Q, Kawagoshi Y, Huang X, Hong N, Van Duc L, Yamashita Y, Hama T (2016) Nitrogen removal properties in a continuous marine anammox bacteria reactor under rapid and extensive salinity changes. Chemosphere 148:444–451. https://doi.org/10.1016/j.chemosphere.2016.01.041
Wu J, Niu Q, Li L, Hu Y, Mribet C, Hojo T, Li Y-Y (2018) A gradual change between methanogenesis and sulfidogenesis during a long-term UASB treatment of sulfate-rich chemical wastewater. Sci Total Environ 636(15):168–176. https://doi.org/10.1016/j.scitotenv.2018.04.172
Xu Y-N, Chen Y (2020) Advances in heavy metal removal by sulfate-reducing bacteria. Water Sci Technol 81(9):1797–1827. https://doi.org/10.2166/wst.2020.227
Ye F, Peng G, Li Y (2011) Influences of influent carbon source on extracellular polymeric substances (EPS) and physicochemical properties of activated sludge. Chemosphere 84(9):1250–1255. https://doi.org/10.1016/j.chemosphere.2011.05.004
Yu L, Huang G, Zhang B, Guo S (2006) Scavenging of Cd through Fe/Mn oxides within natural surface coatings. J Environ Sci 18(6):1199–1203. https://doi.org/10.1016/S1001-0742(06)60062-4
Zagury GJ, Kulnieks VI, Neculita CM (2006) Characterization and reactivity assessment of organic substrates for sulphate-reducing bacteria in acid mine drainage treatment. Chemosphere 64(6):944–954. https://doi.org/10.1016/j.chemosphere.2006.01.001
Zeng Q, Hao T, Hamish RM, Mark CM, van Loosdrecht MCM, Chen G (2019) Recent advances in dissimilatory sulfate reduction: from metabolic study to application. Water Res 150:162–181. https://doi.org/10.1016/j.watres.2018.11.018
Zhang D, Wan J, Pan X (2006) Cadmium sorption by EPSs produced by anaerobic sludge under sulfate-reducing conditions. J Hazard Mater 138(3):589–593. https://doi.org/10.1016/j.jhazmat.2006.05.092
Zhang J, Guo Y, Fang H, Jia W, Li H, Yang L, Wang K (2015) Cadmium sulfide quantum dots stabilized by aromatic amino acids for visible light-induced photocatalytic degradation of organic dyes. New J Chem 39(9):6951–6957. https://doi.org/10.1039/C5NJ00674K
Zhang K, Song L, Dong X (2010) Proteiniclasticum ruminis gen. nov., sp. nov., a strictly anaerobic proteolytic bacterium isolated from yak rumen. Int J Syst Evol Microbiol 60(9):2221–2225. https://doi.org/10.1099/ijs.0.011759-0
Zhang M, Wang H (2016) Preparation of immobilized sulfate reducing bacteria (SRB) granules for effective bioremediation of acid mine drainage and bacterial community analysis. Miner Eng 92:63–71. https://doi.org/10.1016/j.mineng.2016.02.008
Acknowledgements
We thank the financial support from the National Natural Science Foundation of China (52000046; 52060004), Special Project of Guangxi Science and Technology Base and Talent (GuiKe AD20297009; GuiKe AD20297007), Middle-aged and Young Teachers' Basic Ability Promotion Project of Guangxi (2020KY05039; 2021KY0221).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Conceptualization, YJ and XZ; Data curation, JZ and QW; Funding acquisition, YJ, JZ and YZ; Investigation, JZ and YW; Methodology, JZ, QW and YQ; Project administration, YJ, JZ and YZ; Resources, YJ and XZ; Supervision, XZ; Visualization, YZ; Writing—original draft, YZ; writing—review and editing, JZ. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jiang, Y., Zhang, J., Wen, Q. et al. Up-flow anaerobic column reactor for sulfate-rich cadmium-bearing wastewater purification: system performance, removal mechanism and microbial community structure. Biodegradation 33, 239–253 (2022). https://doi.org/10.1007/s10532-022-09983-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-022-09983-0