Abstract
The critical rare earth element dysprosium (Dy) is integral for sustainable technologies. What is concerning is that Dy is in imminent short supply and no current replacements yet exist, coupled with increasing environmental Dy levels influenced by anthropogenic activities. This study applies chemometric methods such as response surface methodology and artificial neural networks to predict low Dy removal levels using the biosorbent Euglena gracilis. A three-factor Box-Behnken experimental design was conducted with initial concentration (1 to 100 µg L−1), contact time (30 to 180 min), and pH (3 to 8) as the three independent variables, and percentage removal and sorption capacity (q) as dependent variables. Using Dy percentage removal as response, for the worst and best conditions ranged from 0 to 92% respectively, with an average removal of 66 ± 4%. Using sorption capacity (q) as a different response variable, q varied from 0 to 93 µg/g with 27 ± 4 µg/g capacity as average. Maximum removal was 92% (q = 93 µg/g) was at pH 3, a contact time of 105 min and at a concentration of 100 µg/L. Using sorption capacity as the response variable for ANOVA, pH and metal concentrations were statistically significant factors, with lower pH and higher metal concentration having improved Dy removal, with a desirability near 1. Statistical tests such as analysis of variance, lack-of-fit, and coefficient of determination (R2) confirmed model validity. A 3–10-1 ANN network array was used to model experimental responses (q). RSM and ANN effectively modeled Dy biosorption. E. gracilis proved to be a cheap and effective biosorbent for Dy biosorption and has the potential to remediate acid mine drainage areas exhibiting low Dy concentrations.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Abdel daiem MM, Hatata A, El-Gohary EH et al (2021) Application of an artificial neural network for the improvement of agricultural drainage water quality using a submerged biofilter. Environ Sci Pollut Res 28:5854–5866. https://doi.org/10.1007/s11356-020-10964-0
Ahmad W, Khan A, Ali N et al (2021) Photocatalytic degradation of crystal violet dye under sunlight by chitosan-encapsulated ternary metal selenide microspheres. Environ Sci Pollut Res 28:8074–8087. https://doi.org/10.1007/s11356-020-10898-7
Allahkarami E, Rezai B (2019) Removal of cerium from different aqueous solutions using different adsorbents: a review. Process Saf Environ Prot 124:345–362. https://doi.org/10.1016/j.psep.2019.03.002
Ambaye TG, Vaccari M, Castro FD et al (2020) Emerging technologies for the recovery of rare earth elements (REEs) from the end-of-life electronic wastes: a review on progress, challenges, and perspectives. Environ Sci Pollut Res 27:36052–36074. https://doi.org/10.1007/s11356-020-09630-2
Amdoun R, Benyoussef E-H, Benamghar A, Khelifi L (2019) Prediction of hyoscyamine content in Datura stramonium L. hairy roots using different modeling approaches: response surface methodology (RSM), artificial neural network (ANN) and kriging. Biochem Eng J 144:8–17. https://doi.org/10.1016/j.bej.2019.01.002
Ameer K, Bae S-W, Jo Y et al (2017) Optimization of microwave-assisted extraction of total extract, stevioside and rebaudioside-A from Stevia rebaudiana (Bertoni) leaves, using response surface methodology (RSM) and artificial neural network (ANN) modelling. Food Chem 229:198–207. https://doi.org/10.1016/j.foodchem.2017.01.121
Bankar A, Nagaraja G (2018) Recent Trends in Biosorption of Heavy Metals by Actinobacteria. In: Singh BP, Gupta VK, Passari AK (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, Amsterdam, pp 257–275
Behera SK, Meena H, Chakraborty S, Meikap BC (2018) Application of response surface methodology (RSM) for optimization of leaching parameters for ash reduction from low-grade coal. Int J Min Sci Technol 28:621–629. https://doi.org/10.1016/j.ijmst.2018.04.014
Bezerra MA, Ferreira SLC, Novaes CG et al (2019) Simultaneous optimization of multiple responses and its application in analytical chemistry – a review. Talanta 194:941–959. https://doi.org/10.1016/j.talanta.2018.10.088
Bigham JM, Cravotta CAI (2016) Acid mine drainage. In: Lal R (ed) Encyclopedia of Soil Science, 3rd edn. CRC Press, Taylor & Francis LLC, Boca Raton, pp 6–10. https://doi.org/10.1081/E-ESS3-120053867
Brewer A, Chang E, Park DM et al (2019) Recovery of rare earth elements from geothermal fluids through bacterial cell surface adsorption. Environ Sci Technol 53:7714–7723. https://doi.org/10.1021/acs.est.9b00301
Cao Y, Shao P, Chen Y et al (2021) A critical review of the recovery of rare earth elements from wastewater by algae for resources recycling technologies. Resour Conserv Recycl 169:105519. https://doi.org/10.1016/j.resconrec.2021.105519
Chaker H, Ameur N, Saidi-Bendahou K et al (2021) Modeling and Box-Behnken design optimization of photocatalytic parameters for efficient removal of dye by lanthanum-doped mesoporous TiO2. J Environ Chem Eng 9:104584. https://doi.org/10.1016/j.jece.2020.104584
da Costa TB, da Silva MGC, Vieira MGA (2021) Recovery of dysprosium by biosorption onto a biocomposite from sericin and alginate. J Water Process Eng 44:102388. https://doi.org/10.1016/j.jwpe.2021.102388
Dev S, Sachan A, Dehghani F et al (2020) Mechanisms of biological recovery of rare-earth elements from industrial and electronic wastes: a review. Chem Eng J 397:124596. https://doi.org/10.1016/j.cej.2020.124596
Devi AP, Mishra PM (2019) Biosorption of dysprosium (III) using raw and surface-modified bark powder of Mangifera indica: isotherm, kinetic and thermodynamic studies. Environ Sci Pollut Res 26:6545–6556. https://doi.org/10.1007/s11356-018-04098-7
Ebrahimi-Najafabadi H, Leardi R, Jalali-Heravi M (2014) Experimental design in analytical chemistry—part i: theory. J AOAC Int 97:3–11. https://doi.org/10.5740/jaoacint.SGEEbrahimi1
Ezechi EH, Muda K (2019) Optimization of methylene blue biosorption and mass transfer resistance on Gardenia carinata activated carbon. DWT 158:343–352. https://doi.org/10.5004/dwt.2019.24243
Fabre E, Henriques B, Viana T et al (2021) Optimization of Nd(III) removal from water by Ulva sp. and Gracilaria sp. through Response Surface Methodology. J Environ Chem Eng 9:105946. https://doi.org/10.1016/j.jece.2021.105946
Fagundez JLS, Salau NPG (2021) Optimization-based artificial neural networks to fit the isotherm models parameters of aqueous-phase adsorption systems. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-17244-5
Ferreira N, Fabre E, Henriques B et al (2021) Response surface approach to optimize the removal of the critical raw material dysprosium from water through living seaweeds. J Environ Manage 300:113697. https://doi.org/10.1016/j.jenvman.2021.113697
Fomina M, Gadd GM (2014) Biosorption: current perspectives on concept, definition and application. Bioresour Technol 160:3–14. https://doi.org/10.1016/j.biortech.2013.12.102
Freitas R, Cardoso CED, Costa S et al (2020) New insights on the impacts of e-waste towards marine bivalves: the case of the rare earth element Dysprosium. Environ Pollut 260:113859. https://doi.org/10.1016/j.envpol.2019.113859
Gallardo K, Castillo R, Mancilla N, Remonsellez F (2020) Biosorption of rare-earth elements from aqueous solutions using walnut shell. Front Chem Eng 2:4. https://doi.org/10.3389/fceng.2020.00004
Gałuszka A, Migaszewski ZM, Pelc A et al (2020) Trace elements and stable sulfur isotopes in plants of acid mine drainage area: implications for revegetation of degraded land. J Environ Sci 94:128–136. https://doi.org/10.1016/j.jes.2020.03.041
Giese EC (2020) Biosorption as green technology for the recovery and separation of rare earth elements. World J Microbiol Biotechnol 36:52. https://doi.org/10.1007/s11274-020-02821-6
Gilman J, Walls L, Bandiera L, Menolascina F (2021) Statistical design of experiments for synthetic biology. ACS Synth Biol 10:1–18. https://doi.org/10.1021/acssynbio.0c00385
Gissibl A, Sun A, Care A et al (2019) Bioproducts From Euglena gracilis: synthesis and applications. Front Bioeng Biotechnol 7:108. https://doi.org/10.3389/fbioe.2019.00108
Gupta NK, Gupta A, Ramteke P et al (2019) Biosorption-a green method for the preconcentration of rare earth elements (REEs) from waste solutions: a review. J Mol Liq 274:148–164. https://doi.org/10.1016/j.molliq.2018.10.134
Gustafsson JP (2010) Visual MINTEQ Version 3.10. Visual MINTEQ – a Free equilibrium speciation model. Stockholm, Sweden
Gwenzi W, Mangori L, Danha C et al (2018) Sources, behaviour, and environmental and human health risks of high-technology rare earth elements as emerging contaminants. Sci Total Environ 636:299–313. https://doi.org/10.1016/j.scitotenv.2018.04.235
Hadiani MR, Khosravi-Darani K, Rahimifard N, Younesi H (2018) Assessment of mercury biosorption by Saccharomyces cerevisiae: response surface methodology for optimization of low Hg (II) concentrations. J Environ Chem Eng 6:4980–4987. https://doi.org/10.1016/j.jece.2018.07.034
Heilmann M, Breiter R, Becker AM (2021) Towards rare earth element recovery from wastewaters: biosorption using phototrophic organisms. Appl Microbiol Biotechnol 105:5229–5239. https://doi.org/10.1007/s00253-021-11386-9
Heimburger A, Tharaud M, Monna F et al (2013) SLRS-5 elemental concentrations of thirty-three uncertified elements deduced from SLRS-5/SLRS-4 ratios. Geostand Geoanalytical Res 37:77–85. https://doi.org/10.1111/j.1751-908X.2012.00185.x
Henriques B, Morais T, Cardoso CED et al (2021) Can the recycling of europium from contaminated waters be achieved through living macroalgae? Study on accumulation and toxicological impacts under realistic concentrations. Sci Total Environ 786:147176. https://doi.org/10.1016/j.scitotenv.2021.147176
Hussain Z, Kim S, Cho J et al (2021) Repeated recovery of rare earth elements using a highly selective and thermo‐responsive genetically encoded polypeptide. Adv Funct Materials 2109158. https://doi.org/10.1002/adfm.202109158
Inwongwan S, Kruger NJ, Ratcliffe RG, O’Neill EC (2019) Euglena central metabolic pathways and their subcellular locations. Metabolites 9:E115. https://doi.org/10.3390/metabo9060115
Ismail LS, Khalili FI (2021) Biosorption of neodymium(III) and cerium(III) ions by loquat leave (Eriobotrya japonica) kinetics and thermodynamic studies. Desalin Water Treat 229:291–301. https://doi.org/10.5004/dwt.2021.27371
Jaafari J, Yaghmaeian K (2019) Optimization of heavy metal biosorption onto freshwater algae (Chlorella coloniales) using response surface methodology (RSM). Chemosphere 217:447–455. https://doi.org/10.1016/j.chemosphere.2018.10.205
Jadhao PR, Mishra S, Pandey A et al (2021) Biohydrometallurgy: a sustainable approach for urban mining of metals and metal refining. In: Pant KK, Gupta SK, Ahmad E (eds) Catalysis for Clean Energy and Environmental Sustainability: Biomass Conversion and Green Chemistry -, vol 1. Springer International Publishing, Cham, pp 865–892
Jalal FE, Xu Y, Li X et al (2021) Fractal approach in expansive clay-based materials with special focus on compacted GMZ bentonite in nuclear waste disposal: a systematic review. Environ Sci Pollut Res 28:43287–43314. https://doi.org/10.1007/s11356-021-14707-7
Jasso-Chávez R, Campos-García ML, Vega-Segura A et al (2021) Microaerophilia enhances heavy metal biosorption and internal binding by polyphosphates in photosynthetic Euglena gracilis. Algal Research 5858:102384. https://doi.org/10.1016/j.algal.2021.102384
Jena A, Pradhan S, Mishra S, Sahoo NK (2021) Evaluation of europium biosorption using Deinococcus radiodurans. Environ Process 8:251–265. https://doi.org/10.1007/s40710-020-00479-8
Jowitt SM, Werner TT, Weng Z, Mudd GM (2018) Recycling of the rare earth elements. Curr Opin Green Sustain Chem 13:1–7. https://doi.org/10.1016/j.cogsc.2018.02.008
Khatiwada B, Hasan MT, Sun A et al (2020) Proteomic response of Euglena gracilis to heavy metal exposure – identification of key proteins involved in heavy metal tolerance and accumulation. Algal Res 45:101764. https://doi.org/10.1016/j.algal.2019.101764
Kowalczyk P, Ligas B, Skrzypczak D et al (2021) Biosorption as a method of biowaste valorization to feed additives: RSM optimization. Environ Pollut 268:115937. https://doi.org/10.1016/j.envpol.2020.115937
Kumari M, Gupta SK (2019) Response surface methodological (RSM) approach for optimizing the removal of trihalomethanes (THMs) and its precursor’s by surfactant modified magnetic nanoadsorbents (sMNP) - an endeavor to diminish probable cancer risk. Sci Rep 9:18339. https://doi.org/10.1038/s41598-019-54902-8
Kusrini E, Kinastiti DD, Wilson L et al (2018) Adsorption of lanthanide ions from aqueous solution in multicomponent systems using activated carbon from banana peels (Musa paradisiaca L.). IJTech 9:1132. https://doi.org/10.14716/ijtech.v9i6.2361
Lewis A, Guéguen C (2020) How growth conditions of Euglena gracilis cells influence cellular composition as evidenced by Fourier transform infrared spectroscopy and direct infusion high-resolution mass spectrometry. J Appl Phycol 32:153–163. https://doi.org/10.1007/s10811-019-01929-z
Leybourne MI, Johannesson KH (2008) Rare earth elements (REE) and yttrium in stream waters, stream sediments, and Fe-Mn oxyhydroxides: fractionation, speciation, and controls over REE + Y patterns in the surface environment. Geochem Cosmochim Acta 72:5962–5983
Lima AT, Ottosen L (2021) Recovering rare earth elements from contaminated soils: critical overview of current remediation technologies. Chemosphere 265:129163. https://doi.org/10.1016/j.chemosphere.2020.129163
Mahapatra DM, Chanakya HN, Ramachandra TV (2013) Euglena sp. as a suitable source of lipids for potential use as biofuel and sustainable wastewater treatment. J Appl Phycol 25:855–865. https://doi.org/10.1007/s10811-013-9979-5
Manikandan A, Suresh Babu P, Shyamalagowri S et al (2021) Emerging role of microalgae in heavy metal bioremediation. J Basic Microbiol jobm.202100363. https://doi.org/10.1002/jobm.202100363
Matho C, Schwarzenberger K, Eckert K et al (2019) Bio-compatible flotation of Chlorella vulgaris: study of zeta potential and flotation efficiency. Algal Res 44:101705. https://doi.org/10.1016/j.algal.2019.101705
Minoda A, Sawada H, Suzuki S et al (2015) Recovery of rare earth elements from the sulfothermophilic red alga Galdieria sulphuraria using aqueous acid. Appl Microbiol Biotechnol 99:1513–1519. https://doi.org/10.1007/s00253-014-6070-3
Mohamed WٍSED, Hamad MTMH, Kamel MZ (2020) Application of statistical response surface methodology for optimization of fluoride removal efficiency by Padina sp. alga. Water Environ Res 92:1080–1088. https://doi.org/10.1002/wer.1305
Moreira VR, Lebron YAR, de Souza Santos LV (2020) Predicting the biosorption capacity of copper by dried Chlorella pyrenoidosa through response surface methodology and artificial neural network models. Chem Eng J Adv 4:100041. https://doi.org/10.1016/j.ceja.2020.100041
Moreno-Sánchez R, Rodríguez-Enríquez S, Jasso-Chávez R et al (2017) Biochemistry and physiology of heavy metal resistance and accumulation in euglena. In: Schwartzbach SD, Shigeoka S (eds) Euglena: Biochemistry, Cell and Molecular Biology. Springer International Publishing, Cham, pp 91–121
Opare EO, Struhs E, Mirkouei A (2021) A comparative state-of-technology review and future directions for rare earth element separation. Renewable and Sustainable Energy Reviews 143:110917. https://doi.org/10.1016/j.rser.2021.110917
Ngwenya BT, Mosselmans JFW, Magennis M et al (2009) Macroscopic and spectroscopic analysis of lanthanide adsorption to bacterial cells. Geochim Cosmochim Acta 73:3134–3147. https://doi.org/10.1016/j.gca.2009.03.018
Parmar P, Shukla A, Goswami D et al (2020) Optimization of cadmium and lead biosorption onto marine Vibrio alginolyticus PBR1 employing a Box-Behnken design. Chem Eng J Adv 4:100043. https://doi.org/10.1016/j.ceja.2020.100043
Pereao O, Bode-Aluko C, Fatoba O et al (2018) Rare earth elements removal techniques from water/wastewater: a review. Desalin Water Treat 130:71–86. https://doi.org/10.5004/dwt.2018.22844
Pereira LMS, Milan TM, Tapia-Blácido DR (2021) Using response surface methodology (RSM) to optimize 2G bioethanol production: a review. Biomass Bioenergy 151:106166. https://doi.org/10.1016/j.biombioe.2021.106166
Podstawczyk D, Dawiec A, Witek-Krowiak A, Chojnacka K (2017) New trends in microbial biosorption modeling and optimization. In: Das S, Dash HR (eds) Handbook of Metal-Microbe Interactions and Bioremediation. CRC Press, Boca Raton, pp 173–199
Rahman N, Nasir M (2018) Application of Box-Behnken design and desirability function in the optimization of Cd(II) removal from aqueous solution using poly(o-phenylenediamine)/hydrous zirconium oxide composite: equilibrium modeling, kinetic and thermodynamic studies. Environ Sci Pollut Res 25:26114–26134. https://doi.org/10.1007/s11356-018-2566-1
Royer-Lavallée A, Neculita CM, Coudert L (2020) Removal and potential recovery of rare earth elements from mine water. J Ind Eng Chem 89:47–57. https://doi.org/10.1016/j.jiec.2020.06.010
Salehi P, Tajabadi FM, Younesi H, Dashti Y (2014) Optimization of lead and nickel biosorption by Cystoseira trinodis (brown algae) using response surface methodology: optimization of lead and nickel biosorption by C. trinodis. Clean Soil Air Water 42:243–250. https://doi.org/10.1002/clen.201100429
Sedlakova-Kadukova J, Kopcakova A, Gresakova L et al (2019) Bioaccumulation and biosorption of zinc by a novel Streptomyces K11 strain isolated from highly alkaline aluminium brown mud disposal site. Ecotoxicol Environ Saf 167:204–211. https://doi.org/10.1016/j.ecoenv.2018.09.123
Squadrone S, Brizio P, Stella C et al (2019) Rare earth elements in marine and terrestrial matrices of Northwestern Italy: implications for food safety and human health. Sci Total Environ 660:1383–1391. https://doi.org/10.1016/j.scitotenv.2019.01.112
Smichowski P, Londonio A (2020) A retrospective and prospective of the use of bio- and nanomaterials for preconcentration, speciation, and determination of trace elements: a review spanning 25 years of research. Anal Bioanal Chem 412:6023–6036. https://doi.org/10.1007/s00216-020-02536-5
Sultana N, Hossain SMZ, Mohammed ME et al (2020) Experimental study and parameters optimization of microalgae based heavy metals removal process using a hybrid response surface methodology-crow search algorithm. Sci Rep 10:15068. https://doi.org/10.1038/s41598-020-72236-8
Wang Y, Seppänen-Laakso T, Rischer H, Wiebe MG (2018) Euglena gracilis growth and cell composition under different temperature, light and trophic conditions. PLoS ONE 13:e0195329. https://doi.org/10.1371/journal.pone.0195329
Winters C, Guéguen C, Noble A (2017) Equilibrium and kinetic studies of Cu(II) and Ni(II) sorption on living Euglena gracilis. J Appl Phycol 29:1391–1398. https://doi.org/10.1007/s10811-016-1040-z
Witek-Krowiak A, Chojnacka K, Podstawczyk D et al (2014) Application of response surface methodology and artificial neural network methods in modelling and optimization of biosorption process. Bioresour Technol 160:150–160. https://doi.org/10.1016/j.biortech.2014.01.021
Xia L, Xu X, Zhu W et al (2015) A comparative study on the biosorption of Cd2+ onto Paecilomyces lilacinus XLA and Mucoromycote sp.XLC. IJMS 16:15670–15687. https://doi.org/10.3390/ijms160715670
Zolgharnein J, Shahmoradi A, Ghasemi JB (2013) Comparative study of Box-Behnken, central composite, and Doehlert matrix for multivariate optimization of Pb (II) adsorption onto Robinia tree leaves: multivariate optimization. J Chemometrics 27:12–20. https://doi.org/10.1002/cem.2487
Acknowledgements
We would like to thank Phillip Siambi from the Noblegen Inc. for the technical assistance and advice in algal culturing, and Aaron Woodcock for aiding with experiments. We would like to acknowledge Dr. Yue Zhao, Stéphanie Beaumont and Chaza Al Akoumy (Université de Sherbrooke) for their help with the zeta potential analysis. We are grateful to the editor and the reviewers for their valuable comments which greatly improved the manuscript.
Funding
This work was supported by the Natural Sciences and Engineering Research Council of Canada, and the Canada Foundation for Innovation.
Author information
Authors and Affiliations
Contributions
AL and CG contributed to the study conception and design. Material preparation, data collection, formal analysis, and visualization were performed by AL. Zeta potential was done by SB. Funding acquisition, project administration, resources, supervision, and visualization were done by CG. The first draft of the manuscript was written by AL, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
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
About this article
Cite this article
Lewis, A., Guéguen, C. Using chemometric models to predict the biosorption of low levels of dysprosium by Euglena gracilis. Environ Sci Pollut Res 29, 58936–58949 (2022). https://doi.org/10.1007/s11356-022-19918-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-19918-0