Abstract
Microbially induced manganese carbonate precipitation has been utilized for the treatment of wastewater containing manganese. In this study, Virgibacillus dokdonensis was used to remove manganese ions from an environment containing 5% NaCl. The results showed a significant decrease in carbonic anhydrase activity and concentrations of carbonate and bicarbonate ions with increasing manganese ion concentrations. However, the levels of humic acid analogues, polysaccharides, proteins, and DNA in EPS were significantly elevated compared to those in a manganese-free environment. The rhodochrosite exhibited a preferred growth orientation, abundant morphological features, organic elements including nitrogen, phosphorus, and sulfur, diverse protein secondary structures, as well as stable carbon isotopes displaying a stronger negative bias. The presence of manganese ions was found to enhance the levels of chemical bonds O–C=O and N–C=O in rhodochrosite. Additionally, manganese in rhodochrosite exhibited both + 2 and + 3 valence states. Rhodochrosite forms not only on the cell surface but also intracellularly. After being treated with free bacteria for 20 days, the removal efficiency of manganese ions ranged from 88.4 to 93.2%, and reached a remarkable 100% on the 10th day when using bacteria immobilized on activated carbon fiber that had been pre-cultured for three days. The removal efficiency of manganese ions was significantly enhanced under the action of pre-cultured immobilized bacteria compared to non-pre-cultured immobilized bacteria. This study contributes to a comprehensive understanding of the mineralization mechanism of rhodochrosite, thereby providing an economically and environmentally sustainable biological approach for treating wastewater containing manganese.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data presented in this study are available on request from the corresponding authors.
References
Amorim SS, Ruas FAD, Barboza NR, de Oliveira Neves VG, Leao VA, Guerra-Sa R (2018) Manganese (Mn2+) tolerance and biosorption by Meyerozyma guilliermondii and Meyerozyma caribbica strains. J Environ Chem Eng 6(4):4538–4545. https://doi.org/10.1016/j.jece.2018.06.061
Awual MR, Alharthi NH, Okamoto Y, Karim MR, Halim ME, Hasan MM, Rahman MM, Islam MM (2017) Ligand field effect for Dysprosium(III) and Lutetium(III) adsorption and EXAFS coordination with novel composite nanomaterials. Chem Eng J 320:427–435. https://doi.org/10.1016/j.cej.2017.03.075
Blakemore RP (1975) Magnetotactic bacteria. Science 190:377–379. https://doi.org/10.1126/science.170679
Cao X, Harris WG, Josan MS, Nair VD (2007) Inhibition of calcium phosphate precipitation under environmentally-relevant conditions. Sci Total Environ 383(1–3):205–215. https://doi.org/10.1016/j.scitotenv.2007.05.012
Castro-Alonso MJ, Montañez-Hernandez LE, Sanchez-Muñoz MA, Macias Franco MR, Narayanasamy R, Balagurusamy N (2019) Microbially induced calcium carbonate precipitation (MICP) and its potential in bioconcrete: microbiological and molecular concepts. Front Mater 6:126. https://doi.org/10.3389/fmats.2019.00126
Cölfen H, Antonietti M (1998) Crystal design of calcium carbonate microparticles using double-hydrophilic block copolymers. Langmuir 14:582–589. https://doi.org/10.1021/la970765t
Debiemme-Chouvy C, Haskouri S, Cachet H (2007) Study by XPS of the chlorination of proteins aggregated onto tin dioxide during electrochemical production of hypochlorous acid. Appl Surf Sci 253(12):5506–5510. https://doi.org/10.1016/j.apsusc.2006.12.077
Dong Y, Zhang Y, Tu B, Miao J (2014) Immobilization of ammonia-oxidizing bacteria by calcium alginate. Ecol Eng 73:809–814. https://doi.org/10.1016/j.ecoleng.2014.09.020
Duan X, Lian J, Ma J, Kim T, Zheng W (2010) Shape-controlled synthesis of metal carbonate nanostructure via ionic liquid-assisted hydrothermal route: the case of manganese carbonate. Cryst Growth Des 10(10):4449–4455. https://doi.org/10.1021/cg1006567
Eltarahony M, Zaki S, Abd-El-Haleem D (2020) Aerobic and anaerobic removal of lead and mercury via calcium carbonate precipitation mediated by statistically optimized nitrate reductases. Sci Rep 10(1):4029. https://doi.org/10.1038/s41598-020-60951-1
Eltarahony M, El-Fakharany E, Abu-Serie M, ElKady M, Ibrahim A (2021a) Statistical modeling of methylene blue degradation by yeast-bacteria consortium; optimization via agro-industrial waste, immobilization and application in real effluents. Microb Cell Factories 20(1):1–26. https://doi.org/10.1186/s12934-021-01730-z
Eltarahony M, Kamal A, Zaki S, Abd-El-Haleem D (2021b) Heavy metals bioremediation and water softening using ureolytic strains Metschnikowia pulcherrima and Raoultella planticola. J Chem Technol Biotechnol 96(11):3152–3165. https://doi.org/10.1002/jctb.6868
Fan Y, Su J, Zheng Z, Gao J, Ali A (2021) Denitrification performance and mechanism of a novel isolated Acinetobacter sp. FYF8 in oligotrophic ecosystem. Bioresour Technol 320:124280. https://doi.org/10.1016/j.biortech.2020.124280
Frankel RB, Bazylinski DA (2003) Biologically induced mineralization by bacteria. Rev Mineral Geochem 54:95–114. https://doi.org/10.2113/0540095
Freedman DE, Riley SM, Jones ZL, Rosenblum JS, Sharp JO, Spear JR, Cath TY (2017) Biologically active filtration for fracturing flowback and produced water treatment. J Water Process Eng 18:29–40. https://doi.org/10.1016/j.jwpe.2017.05.008
Han Z, Li D, Zhao H, Yan H, Li P (2017) Precipitation of carbonate minerals induced by the Halophilic Chromohalobacter israelensis under high salt concentrations: implications for natural environments. Minerals 7:95. https://doi.org/10.3390/min7060095
Hatayama K (2020) Manganese carbonate precipitation induced by calcite-forming bacteria. Geomicrobiol J 37(7):603–609. https://doi.org/10.1080/01490451.2020.1743391
Hu JL, Zeng Q, Chen HY, Dong HL (2022) Effect of bacterial cell addition on Fe(III) reduction and soil organic matter transformation in a farmland soil. Geochim Cosmochim Acta 325:25–38. https://doi.org/10.1016/j.gca.2022.03.018
Huang P, Xing BG, Fang JL, Tang WX (1998) Secondary structure of rabbit Cd5Zn2MT-II, Zn7MT-II and Pt7MT-II by Fourier transform infrared spectroscopy. Spectrosc Lett 31(7):1599–1608. https://doi.org/10.1080/00387019808001663
Huang LJ, Li FC, Ji C, Wang YZ, Yang GG (2022) Carbon isotope fractionation and its tracer significance to carbon source during precipitation of calcium carbonate in the presence of Bacillus cereus LV-1. Chem Geol 609:121029. https://doi.org/10.1016/j.chemgeo.2022.121029
Ibrahim A, El-Fakharany EM, Abu-Serie MM, ElKady MF, Eltarahony M (2022) Methyl orange biodegradation by immobilized consortium microspheres: experimental design approach, toxicity study and bioaugmentation potential. Biology 11(1):76. https://doi.org/10.3390/biology11010076
Jiang C, Guo Z, Zhu Y, Liu H, Wan M, Jiang L (2015) Shewanella-mediated biosynthesis of manganese oxide micro-/nanocubes as efficient electrocatalysts for the oxygen reduction reaction. Chemsuschem 8(1):158–163. https://doi.org/10.1002/cssc.201402759
Juve J-MA, Christensen FMS, Wang Y, Wei Z (2022) Electrodialysis for metal removal and recovery: a review. Chem Eng J 435:134857. https://doi.org/10.1016/j.cej.2022.134857
Kaushal M, Wani SP (2016) Plant-growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol 66:35–42. https://doi.org/10.1007/s13213-015-1112-3
Kimber RL, Lewis EA, Parmeggiani F, Smith K, Bagshaw H, Starborg T, Joshi N, Figueroa AI, van der Laan G, Cibin G, Gianolio D, Haigh SJ, Pattrick RAD, Turner NJ, Lloyd JR (2018) Biosynthesis and characterization of copper nanoparticles using Shewanella oneidensis: application for click chemistry. Small 14(10):1703145. https://doi.org/10.1002/smll.201703145
Kong J, Yu S (2007) Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim Biophys Sin 39(8):549–559. https://doi.org/10.1111/j.1745-7270.2007.00320.x
Kuo CL, Wu YQ (1980) An X-ray method of determining the degree of preferred orientation of ferroelectric material with layer type structure after hot-pressing. Acta Phys Sin 12: 1640–1644. http://wulixb.iphy.ac.cn/CN/Y1980/V29/I12/1640
Lee HK, Sakemi D, Selyanchyn R, Lee CG, Lee SW (2014) Titania nanocoating on MnCO3 microspheres via liquid-phase deposition for fabrication of template-assisted core–shell- and hollow-structured composites. ACS Appl Mater Interfaces 6(1):57–64. https://doi.org/10.1021/am404052p
Lei Y, Saakes M, van der Weijden RD, Buisman CJN (2020) Electrochemically mediated calcium phosphate precipitation from phosphonates: implications on phosphorus recovery from non-orthophosphate. Water Res 169:115206. https://doi.org/10.1016/j.watres.2019.115206
Li D, Li R, Ding Z, Ruan X, Tang J (2020) Discovery of a novel native bacterium of Providencia sp. with high biosorption and oxidation ability of manganese for bioleaching of heavy metal contaminated soils. Chemosphere 241:125039. https://doi.org/10.1016/j.chemosphere.2019.125039
Liao X, Sun S, Zhou S, Ye M, Liang J, Huang J, Guan Z, Li S (2019) A new strategy on biomining of low grade base-metal sulfide tailings. Bioresour Technol 294:122187. https://doi.org/10.1016/j.biortech.2019.122187
Lindskog S (1997) Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74(1):1–20. https://doi.org/10.1016/s0163-7258(96)00198-2
Liu B, Zhang Y, Lu M, Su Z, Li G, Jiang T (2019) Extraction and separation of manganese and iron from ferruginous manganese ores: a review. Miner Eng 131:286–303. https://doi.org/10.1016/j.mineng.2018.11.016
Liu Y, Ali A, Su J-F, Li K, Hu R-Z, Wang Z (2023) Microbial-induced calcium carbonate precipitation: influencing factors, nucleation pathways, and application in waste water remediation. Sci Total Environ 860:160439. https://doi.org/10.1016/j.scitotenv.2022.160439
Lopes WA, Fascio M (2004) Esquema para interpretação de espectros de substâncias orgânicas na região do infravermelho. Quim Nova 27(4):670–673. https://doi.org/10.1590/S0100-40422004000400025
Luo Z, Shu J, Chen M, Wang R, Zeng X, Yang Y, Wang R, Chen S, Liu R, Liu Z, Sun Z, Yu K, Deng Y (2021) Enhanced leaching of manganese from low-grade pyrolusite using ball milling and electric field. Ecotoxicol Environ Saf 211:111893. https://doi.org/10.1016/j.ecoenv.2021.111893
Makarova MV, Artemenko A, Kopecek J, Laufek F, Zemenova P, Trepakov VA, Dejneka A (2016) Thermal stability of perovskite phase in heavily Mn-doped SrTiO3 nanoparticles in oxidizing and reducing atmospheres. Scr Mater 116:21–25. https://doi.org/10.1016/j.scriptamat.2016.01.029
Mezzaroba L, Alfieri DF, Simão ANC, Reiche EMV (2019) The role of zinc, copper, manganese and iron in neurodegenerative diseases. Neurotoxicology 74:230–241. https://doi.org/10.1016/j.neuro.2019.07.007
Naik-Samant S, Furtado I (2019) Formation of rhodochrosite by Haloferax alexandrinus GUSF-1. J Clust Sci 30:1435–1441. https://doi.org/10.1007/s10876-019-01586-9
Nassrallah-Aboukais N, Boughriet A, Gengembre L, Aboukais A (1998) Manganese(II)/vaterite/water systems spectroscopic and thermodynamic study. J Chem Soc Faraday Trans 94(16):2399–2405. https://doi.org/10.1039/A803668C
Obst M, Dynes JJ, Lawrence JR, Swerhone GD, Benzerara K, Karunakaran C, Kaznatcheev K, Tyliszczak T, Hitchcock AP (2009) Precipitation of amorphous CaCO3 (aragonite-like) by cyanobacteria: a STXM study of the influence of EPS on the nucleation process. Geochim Cosmochim Acta 73(14):4180–4198. https://doi.org/10.1016/j.gca.2009.04.013
Ojedokun AT, Bello OS (2016) Sequestering heavy metals from wastewater using cow dung. Water Resour Ind 13:7–13. https://doi.org/10.1016/j.wri.2016.02.002
Oku M, Hirokawa K, Ikeda S (1975) X-ray photoelectron spectroscopy of manganese-oxygen systems. J Electron Spectrosc Relat Phenom 7(5):465–473. https://doi.org/10.1016/0368-2048(75)85010-9
Osaki S (1973) Carbon and oxygen isotopic compositions of hydrothermal rhodochrosites from Oe, Inakuraishi and Jokoku Mines, Hokkaido, Japan. Geochem J 6(4):151–162. https://doi.org/10.2343/geochemj.6.151
Paulo C, Kenney J, Persson P, Dittrich M (2018) Effects of phosphorus in growth media on biomineralization and cell surface properties of marine cyanobacteria Synechococcus. Geosciences (switz) 8(12):471. https://doi.org/10.3390/geosciences8120471
Perri E, Tucker M, Słowakiewicz M, Whitaker F, Bowen L, Perrotta I (2018) Carbonate and silicate biomineralization in a hypersaline microbial mat (Mesaieed Sabkha, Qatar): roles of bacteria, extracellular polymeric substances and viruses. Sedimentology 65:1213–1245. https://doi.org/10.1111/sed.12419
Qasem NAA, Mohammed RH, Lawal DU (2021) Removal of heavy metal ions from wastewater: a comprehensive and critical review. NPJ Clean Water 4(1):36. https://doi.org/10.1038/s41545-021-00127-0
Rajasekar A, Wilkinson S, Moy CKS (2021) MICP as a potential sustainable technique to treat or entrap contaminants in the natural environment: a review. ESE 6:100096. https://doi.org/10.1016/j.ese.2021.100096
Rohde M, Mayer H (2007) Exocytotic process as a novel model for mineralization by osteoblasts in vitro and in vivo determined by electron microscopic analysis. Calcif Tissue Int 80:323–336. https://doi.org/10.1007/s00223-007-9013-5
Sánchez-Román M, Romanek CS, Fernández-Remolar DC, Sánchez-Navas A, McKenzie JA, Pibernat RA, Vasconcelos C (2011) Aerobic biomineralization of Mg-rich carbonates: implications for natural environments. Chem Geol 281(3–4):143–150. https://doi.org/10.1016/j.chemgeo.2010.11.020
Sarvamangala H, Gopal J, Muraleedharan P, George RP, Dayal RK, Natarajan KA (2008) Biomineralization of manganese by Bacillus spp. isolated from a marine biofilm. Min Metall Explor 25(3):149–155. https://doi.org/10.1007/BF03403401
Shafaei A, Rezayee M, Arami M, Nikazar M (2010) Removal of Mn2+ ions from synthetic wastewater by electrocoagulation process. Desalination 260(1–3):23–28. https://doi.org/10.1016/j.desal.2010.05.006
Sherman VR, Yang W, Meyers MA (2015) The materials science of collagen. J Mech Behav Biomed Mater 52:22–50. https://doi.org/10.1016/j.jmbbm.2015.05.023
Shrestha R, Ban S, Devkota S, Sharma S, Joshi R, Tiwari AP, Kim HY, Joshi MK (2021) Technological trends in heavy metals removal from industrial wastewater: a review. J Environ Chem Eng 9(4):105688. https://doi.org/10.1016/j.jece.2021.105688
Singh V, Reddy KVK, Tripathy SK, Kumari P, Dubey AK, Mohanty R, Satpathy RR, Mukherjee S (2021) A sustainable reduction roasting technology to upgrade the ferruginous manganese ores. J Clean Prod 284:124784. https://doi.org/10.1016/j.jclepro.2020.124784
Sternbeck J (1997) Kinetics of rhodochrosite crystal growth at 25 °C: the role of surface speciation. Geochim Cosmochim Acta 61(4):785–793. https://doi.org/10.1016/S0016-7037(96)00379-1
Strieth D, Schwarz A, Stiefelmaier J, Erdmann N, Muffler K, Ulber R (2021) New procedure for separation and analysis of the main components of cyanobacterial EPS. J Biotechnol 328:78–86. https://doi.org/10.1016/j.jbiotec.2021.01.007
Tan BJ, Klabunde KJ, Sherwood PM (1991) XPS studies of solvated metal atom dispersed (SMAD) catalysts. Evidence for layered cobalt–manganese particles on alumina and silica. J Am Chem Soc 113(3):855–861. https://doi.org/10.1021/ja00003a019
Tang Y, Zeiner CA, Santelli CM, Hansel CM (2013) Fungal oxidative dissolution of the Mn(II)-bearing mineral rhodochrosite and the role of metabolites in manganese oxide formation. Environ Microbiol 15(4):1063–1077. https://doi.org/10.1111/1462-2920.12029
Tucker M (2020) Fossil viruses. Geol Today 36:156–160. https://doi.org/10.1111/gto.12321
Yamazaki H, Beniash E, Yamakoshi Y, Simmer JP, Margolis HC (2017) Protein phosphorylation and mineral binding affect the secondary structure of the leucine-rich amelogenin peptide. Front Physiol 8:450. https://doi.org/10.3389/fphys.2017.00450
Yan H, Han Z, Zhao H, Pan J, Zhao Y, Tucker ME, Zhou J, Yan X, Yang H, Fan D (2020) The bio-precipitation of calcium and magnesium ions by free and immobilized Lysinibacillus fusiformis DB1-3 in the wastewater. J Clean Prod 252:119826. https://doi.org/10.1016/j.jclepro.2019.119826
Yan H, Huang M, Wang J, Geng H, Zhang X, Qiu Z, Dai Y, Han Z (2022) Difference in calcium ion precipitation between free and immobilized Halovibrio mesolongii HMY2. J Environ Sci 122:184–200. https://doi.org/10.1016/j.jes.2022.02.002
Yan H, Cao J, Teng M, Meng L, Zhao L, Chi X, Han Z, Tucker ME, Zhao H (2023) Calcium ion removal at different sodium chloride concentrations by free and immobilized halophilic bacteria. Water Res 229:119438. https://doi.org/10.1016/j.watres.2022.119438
Yang Z, Zhang W, Wang Q, Song X, Qian Y (2006) Synthesis of porous and hollow microspheres of nanocrystalline Mn2O3. Chem Phys Lett 418(1–3):46–49. https://doi.org/10.1016/j.cplett.2005.10.076
Zhang B, Sun BS, Jin M, Gong TS, Gao ZH (2007) Extraction and analysis of extracellular polymeric substances in membrane fouling in submerged MBR. Desalination 227:286–294. https://doi.org/10.1016/j.desal.2007.06.032
Zhang RY, Neu TR, Bellenberg S, Kuhlicke U, Sand W, Vera M (2015) Use of lectins to in situ visualize glycoconjugates of extracellular polymeric substances in acidophilic archaeal biofilms. Microb Biotechnol 8(3):448–461. https://doi.org/10.1111/1751-7915.12188
Zhang H, Pan X, Wu Q, Guo J, Wang C, Liu H (2021) Manganese carbonate nanoparticles-mediated mitochondrial dysfunction for enhanced sonodynamic therapy. Exploration 1(2):20210010. https://doi.org/10.1002/EXP.20210010
Zhao Y, Han Z, Yan H, Zhao H, Tucker ME, Gao X, Guo N, Meng R (2021) Selective adsorption of amino acids in crystals of monohydrocalcite induced by the facultative anaerobic Enterobacter ludwigii SYB1. Front Microbiol 12:696557. https://doi.org/10.3389/fmicb.2021.696557
Zhao Y, Wei X, Gao X, Li J, Zhang Y, Hu K, Han C, Wang Q, Han Z (2023) Proto-dolomite spherulites with heterogeneous interior precipitated in brackish water cultivation of freshwater cyanobacterium Leptolyngbya boryana. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2023.167552
Zheng L, Lin H, Dong Y, Li B, Lu Y (2023) A promising approach for simultaneous removal of ammonia and multiple heavy metals from landfill leachate by carbonate precipitating bacterium. J Hazard Mater 456:131662. https://doi.org/10.1016/j.jhazmat.2023.131662
Zhou F, Yan C, Wang H, Sun Q, Wang Q, Alshameri A (2015) Flotation behavior of four C18 hydroxamic acids as collectors of rhodochrosite. Miner Eng 78:15–20. https://doi.org/10.1016/j.mineng.2015.04.006
Zhou X, Zhao F, Zhang P, Yu G (2021) Solar water evaporation toward water purification and beyond. ACS Mater Lett 3(8):1112–1129. https://doi.org/10.1021/acsmaterialslett.1c00304
Zhu Y, Nong P, Mo N, Zhu Z, Deng H, Tang S, Yang H, Li Z, Wang X (2021) Dissolution and solubility of calcite-rhodochrosite solid solutions [(Ca1−xMnx)CO3] at 25 °C. Geochem Trans 22(1):1–20. https://doi.org/10.1186/s12932-021-00075-1
Zhuang D, Yan H, Tucker ME, Zhao H, Han Z, Zhao Y, Sun B, Li D, Pan J, Zhao Y, Meng R, Shan G, Zhang X, Tang R (2018) Calcite precipitation induced by Bacillus cereus MRR2 cultured at different Ca2+ concentrations: Further insights into biotic and abiotic calcite. Chem Geol 500:64–87. https://doi.org/10.1016/j.chemgeo.2018.09.018
Zolotoyabko E (2009) Determination of the degree of preferred orientation within the March-Dollase approach. J Appl Crystallogr 42(3):513–518. https://doi.org/10.1107/S0021889809013727
Zuo W, Yu Y, Huang H (2021) Making waves: microbe-photocatalyst hybrids may provide new opportunities for treating heavy metal polluted wastewater. Water Res 195:116984. https://doi.org/10.1016/j.Watres.2021.116984
Funding
This work was supported by the National Natural Science Foundation of China (42372135, 42072136, 41972108, 42106144); Natural Science Foundation of Shandong Province (ZR2023MD063, ZR2020MC041, ZR2020QD089); Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, Ministry of Natural Resources (HY202306); Foreign visiting scholar funded by Shandong Provincial government.
Author information
Authors and Affiliations
Contributions
Conceptualization, XS; methodology, JW, XC, and CH; software, SJ and LM; validation, YZ and HZ; formal analysis, MT, HY and SJ; investigation, SJ; resources, HY; data curation, SJ and HY; writing—original draft preparation, SJ and HY; writing—review and editing, SJ, HY, HZ, HW, and MT; supervision, HY, ZH, and HW; project administration, HZ; funding acquisition, HZ and HY; visualization, LW, YZ (Yueming Zhao) and HY.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yan, H., Jin, S., Sun, X. et al. Mn2+ recycling in hypersaline wastewater: unnoticed intracellular biomineralization and pre-cultivation of immobilized bacteria. World J Microbiol Biotechnol 40, 57 (2024). https://doi.org/10.1007/s11274-023-03879-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-023-03879-8