Adsorption of cadmium ions using the bioadsorbent of Pichia kudriavzevii YB5 immobilized by polyurethane foam and alginate gels

Zhao, Wenyu; Zhou, Ting; Zhu, Junxiang; Sun, Xun; Xu, Ying

doi:10.1007/s11356-017-0785-5

Research Article
Published: 22 November 2017

Adsorption of cadmium ions using the bioadsorbent of Pichia kudriavzevii YB5 immobilized by polyurethane foam and alginate gels

Wenyu Zhao¹,
Ting Zhou¹,
Junxiang Zhu^1,2,
Xun Sun¹ &
Ying Xu ORCID: orcid.org/0000-0003-1705-1050¹

Environmental Science and Pollution Research volume 25, pages 3745–3755 (2018)Cite this article

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Abstract

Pichia kudriavzevii YB5, mutated from Pichia kudriavzevii A16 with a strong ability to remove cadmium ions, was immobilized by polyurethane foam and alginate gels in this work. The immobilization conditions were optimized as follows: sodium alginate concentration of 2% (w/v), calcium chloride concentration of 2% (w/v), biomass dose of 1 × 10⁹ cell/mL, and cross-linking time for 4 h. Then, the results of batch adsorption experiments showed that the removal capacity of prepared bioadsorbent was significantly affected by the pH of media, contact time, and the initial Cd(II) concentration, and a suitable adsorption conditions of Cd(II) could be achieved with a pH value of 6.0 at 20 °C for 90 min. Kinetic and isothermal results indicated the behavior of Cd(II) adsorption onto immobilized P. kudriavzevii YB5 fitted to the pseudo-second-order kinetic equation and the Langmuir adsorption model. Thermodynamic results showed that the Cd(II) adsorption process was endothermic and spontaneous in nature. Besides, the Cd(II) removing capacity of the prepared bioadsorbent was also tested in the oyster hydrolysates, showing an average removal rate of 54.35%. Thus, the immobilized P. kudriavzevii YB5 adsorbent had great potential for application in aquatic products to ensure the food safety.

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References

Arıca MY, Bayramoǧlu G, Yılmaz M, Bektaş S, Genç Ö (2004) Biosorption of Hg²⁺, Cd²⁺, and Zn²⁺ by Ca-alginate and immobilized wood-rotting fungus Funalia trogii. J Hazard Mater 109(1-3):191–199. https://doi.org/10.1016/j.jhazmat.2004.03.017
Article Google Scholar
Auta M, Hameed BH (2014) Chitosan–clay composite as highly effective and low-cost adsorbent for batch and fixed-bed adsorption of methylene blue. Chem Eng J 237:352–361. https://doi.org/10.1016/j.cej.2013.09.066
CAS Article Google Scholar
Beker MJ, Blumbergs JE, Ventina EJ, Rapoport AI (1984) Characteristics of cellular membranes at rehydration of dehydrated yeast Saccharomyces cerevisiae. Appl Microbiol Biot 19:347–352
Article Google Scholar
Carabajal M, Perullini M, Jobbágy M, Ullrich R, Hofrichter M, Levin L (2016) Removal of phenol by immobilization of Trametes versicolor in silica–alginate–fungus biocomposites and loofa sponge. CLEAN Soil Air Water 44(2):180–188. https://doi.org/10.1002/clen.201400366
CAS Article Google Scholar
Carro L, Barriada JL, Herrero R, de Vicente MES (2015) Interaction of heavy metals with Ca-pretreated Sargassum muticum algal biomass: characterization as a cation exchange process. Chem Eng J 264:181–187. https://doi.org/10.1016/j.cej.2014.11.079
CAS Article Google Scholar
Chen L, Bai B (2013) Equilibrium, kinetic, thermodynamic, and in situ regeneration studies about methylene blue adsorption by the raspberry-like TiO₂@yeast microspheres. Ind Eng Chem Res 52(44):15568–15577. https://doi.org/10.1021/ie4020364
CAS Article Google Scholar
Chiou MS, Li HY (2002) Equilibrium and kinetic modeling of adsorption of reactive dye on cross-linked chitosan beads. J Hazard Mater 93(2):233–248. https://doi.org/10.1016/S0304-3894(02)00030-4
CAS Article Google Scholar
Chojnacka K (2010) Biosorption and bioaccumulation–the prospects for practical applications. Environ Int 36(3):299–307. https://doi.org/10.1016/j.envint.2009.12.001
CAS Article Google Scholar
Clares ME, Guerrero MG, García-González M (2015) Cadmium removal by Anabaena sp. ATCC 33047 immobilized in polyurethane foam. Int J Environ Sci Technol 12(5):1793–1798. https://doi.org/10.1007/s13762-014-0743-4
CAS Article Google Scholar
Congeevaram S, Dhanarani S, Park J, Dexilin M, Thamaraiselvi K (2007) Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. J Hazard Mater 146(1-2):270–277. https://doi.org/10.1016/j.jhazmat.2006.12.017
CAS Article Google Scholar
De Ory I, Romero LE, Cantero D (2004) Optimization of immobilization conditions for vinegar production. Siran, wood chips and polyurethane foam as carriers for Acetobacter aceti. Process Biochem 39(5):547–555. https://doi.org/10.1016/S0032-9592(03)00136-5
Article Google Scholar
Draget KI, Skjåk-Bræk G, Smidsrød O (1997) Alginate based new materials. Int J Biol Macromol 21(1-2):47–55. https://doi.org/10.1016/S0141-8130(97)00040-8
CAS Article Google Scholar
Freundlich H (1907) Über die adsorption in lösungen. Z Phys Chem 57:385–470
CAS Google Scholar
Fu J, Chen Z, Wang M, Liu S, Zhang J, Zhang J, Han R, Xu Q (2015) Adsorption of methylene blue by a high-efficiency adsorbent (polydopamine microspheres): kinetics, isotherm, thermodynamics and mechanism analysis. Chem Eng J 259:53–61. https://doi.org/10.1016/j.cej.2014.07.101
CAS Article Google Scholar
Gallardo JCM, Souza CS, Cicarelli RMB, Oliveira KF, Morais MR, Laluce C (2011) Enrichment of a continuous culture of Saccharomyces cerevisiae with the yeast Issatchenkia orientalis in the production of ethanol at increasing temperatures. J Ind Microbiol Biot 38(3):405–414. https://doi.org/10.1007/s10295-010-0783-9
CAS Article Google Scholar
Gavrilescu M (2004) Removal of heavy metals from the environment by biosorption. Eng Life Sci 4(3):219–232. https://doi.org/10.1002/elsc.200420026
CAS Article Google Scholar
Granato D, de Araújo Calado VM, Jarvis B (2014) Observations on the use of statistical methods in food science and technology. Food Res Int 55:137–149. https://doi.org/10.1016/j.foodres.2013.10.024
Article Google Scholar
Ha J, Engler CR, Wild JR (2009) Biodegradation of coumaphos, chlorferon, and diethylthiophosphate using bacteria immobilized in Ca-alginate gel beads. Bioresour Technol 100(3):1138–1142. https://doi.org/10.1016/j.biortech.2008.08.022
CAS Article Google Scholar
He J, Chen JP (2014) A comprehensive review on biosorption of heavy metals by algal biomass: materials, performances, chemistry, and modeling simulation tools. Bioresour Technol 160:67–78. https://doi.org/10.1016/j.biortech.2014.01.068
CAS Article Google Scholar
Henriques B, Lopes CB, Figueira P, Rocha LS, Duarte AC, Vale C, Pardal MA, Pereira E (2017) Bioaccumulation of Hg, Cd and Pb by Fucus vesiculosus in single and multi-metal contamination scenarios and its effect on growth rate. Chemosphere 171:208–222. https://doi.org/10.1016/j.chemosphere.2016.12.086
CAS Article Google Scholar
Isono N, Hayakawa H, Usami A, Mishima T, Hisamatsu M (2012) A comparative study of ethanol production by Issatchenkia orientalis strains under stress conditions. J Biosci Bioeng 113(1):76–78. https://doi.org/10.1016/j.jbiosc.2011.09.004
CAS Article Google Scholar
Ju YR, Chen WY, Liao CM (2012) Assessing human exposure risk to cadmium through inhalation and seafood consumption. J Hazard Mater 227:353–361
Article Google Scholar
Kılıc M, Kırbıyık C, Çepelioğullar Ö, Pütün AE (2013) Adsorption of heavy metal ions from aqueous solutions by bio-char, a by-product of pyrolysis. Appl Surf Sci 283:856–862. https://doi.org/10.1016/j.apsusc.2013.07.033
Article Google Scholar
Kim JW, Rainina EI, Mulbry WW, Engler CR, Wild JR (2002) Enhanced-rate biodegradation of organophosphate neurotoxins by immobilized nongrowing bacteria. Biotechnol Prog 18(3):429–436. https://doi.org/10.1021/bp0200346
CAS Article Google Scholar
Kuyucak N, Volesky B (1988) Biosorbents for recovery of metals from industrial solutions. Biotechnol Lett 10(2):137–142. https://doi.org/10.1007/BF01024641
CAS Article Google Scholar
Langmuir I (1918) The adsorption of gases on plane surfaces of glass, mica and platinum. J Am Chem Soc 40(9):1361–1403. https://doi.org/10.1021/ja02242a004
CAS Article Google Scholar
Lee KY, Mooney DJ (2012) Alginate: properties and biomedical applications. Prog Polym Sci 37(1):106–126. https://doi.org/10.1016/j.progpolymsci.2011.06.003
CAS Article Google Scholar
Li C, Xu Y, Jiang W, Dong X, Wang D, Liu B (2013) Effect of NaCl on the heavy metal tolerance and bioaccumulation of Zygosaccharomyces rouxii and Saccharomyces cerevisiae. Bioresour Technol 143:46–52. https://doi.org/10.1016/j.biortech.2013.05.114
CAS Article Google Scholar
Li C, Jiang W, Ma N, Zhu Y, Dong X, Wang D, Meng X, Xu Y (2014) Bioaccumulation of cadmium by growing Zygosaccharomyces rouxii and Saccharomyces cerevisiae. Bioresour Technol 155:116–121. https://doi.org/10.1016/j.biortech.2013.12.098
CAS Article Google Scholar
Li C, Yu J, Wang D, Li L, Yang X, Ma H, Xu Y (2016) Efficient removal of zinc by multi-stress-tolerant yeast Pichia kudriavzevii A16. Bioresour Technol 206:43–49. https://doi.org/10.1016/j.biortech.2016.01.057
CAS Article Google Scholar
Liu B, Wang D, Xu Y, Huang G (2011) Adsorption properties of Cd (II)-imprinted chitosan resin. J Mater Sci 46(5):1535–1541. https://doi.org/10.1007/s10853-010-4958-6
CAS Article Google Scholar
Liu RL, Liu Y, Zhou XY, Zhang ZQ, Zhang J, Dang FQ (2014) Biomass-derived highly porous functional carbon fabricated by using a free-standing template for efficient removal of methylene blue. Bioresour Technol 154:138–147. https://doi.org/10.1016/j.biortech.2013.12.034
CAS Article Google Scholar
Lu M, Liu YG, Hu XJ, Ben Y, Zeng XX, Li TT, Wang H (2013) Competitive adsorption of Cu (II) and Pb (II) ions from aqueous solutions by Ca-alginate immobilized activated carbon and Saccharomyces cerevisiae. J Cent South Univ 20(9):2478–2488. https://doi.org/10.1007/s11771-013-1760-z
CAS Article Google Scholar
Macías-Mayorga D, Laiz I, Moreno-Garrido I, Blasco J (2015) Is oxidative stress related to cadmium accumulation in the Mollusc Crassostrea angulata? Aquat Toxicol 161:231–241. https://doi.org/10.1016/j.aquatox.2015.02.007
Article Google Scholar
Modak JM, Natarajan KA (1995) Biosorption of metals using nonliving biomass—a review. Miner Metall Process 12:189–196
CAS Google Scholar
Moreno-Garrido I (2008) Microalgae immobilization: current techniques and uses. Bioresour Technol 99(10):3949–3964. https://doi.org/10.1016/j.biortech.2007.05.040
CAS Article Google Scholar
Oberoi HS, Babbar N, Sandhu SK, Dhaliwal SS, Kaur U, Chadha BS, Bhargav VK (2012) Ethanol production from alkali-treated rice straw via simultaneous saccharification and fermentation using newly isolated thermotolerant Pichia kudriavzevii HOP-1. J Ind Microbiol Biot 39(4):557–566. https://doi.org/10.1007/s10295-011-1060-2
CAS Article Google Scholar
Ong SA, Toorisaka E, Hirata M, Hano T (2013) Comparative study on kinetic adsorption of Cu(II), Cd(II) and Ni(II) ions from aqueous solutions using activated sludge and dried sludge. Appl Water Sci 3(1):321–325. https://doi.org/10.1007/s13201-013-0084-3
CAS Article Google Scholar
Pajic-Lijakovic I, Levic S, Hadnađev M, Stevanovic-Dajic Z, Radosevic R, Nedovic V, Bugarski B (2015) Structural changes of Ca-alginate beads caused by immobilized yeast cell growth. Biochem Eng J 103:32–38. https://doi.org/10.1016/j.bej.2015.06.016
CAS Article Google Scholar
Pan B, Xing B (2010) Adsorption kinetics of 17α-ethinyl estradiol and bisphenol A on carbon nanomaterials. I. Several concerns regarding pseudo-first order and pseudo-second order models. J Soils Sediments 10(5):838–844. https://doi.org/10.1007/s11368-009-0184-8
CAS Article Google Scholar
Rady MM, Hemida KA (2015) Modulation of cadmium toxicity and enhancing cadmium-tolerance in wheat seedlings by exogenous application of polyamines. Ecotoxicol Environ Saf 119:178–185. https://doi.org/10.1016/j.ecoenv.2015.05.008
CAS Article Google Scholar
Smidsrød O, Skja G (1990) Alginate as immobilization matrix for cells. Trends Biotechnol 8(3):71–78. https://doi.org/10.1016/0167-7799(90)90139-O
Article Google Scholar
Srivastava VC, Mall ID, Mishra IM (2007) Adsorption thermodynamics and isosteric heat of adsorption of toxic metal ions onto bagasse fly ash (BFA) and rice husk ash (RHA). Chem Eng J 132(1-3):267–278. https://doi.org/10.1016/j.cej.2007.01.007
CAS Article Google Scholar
Srivastava VC, Mall ID, Mishra IM (2009) Competitive adsorption of cadmium (II) and nickel (II) metal ions from aqueous solution onto rice husk ash. Chem Eng Process Process Intensif 48(1):370–379. https://doi.org/10.1016/j.cep.2008.05.001
CAS Article Google Scholar
Sulaymon AH, Ebrahim SE, Abdullah SM, Al-Musawi TJ (2010) Removal of lead, cadmium, and mercury ions using biosorption. Desalin Water Treat 24(1-3):344–352. https://doi.org/10.5004/dwt.2010.1963
CAS Article Google Scholar
Sun X, Sun C, Zhang X, Zhang H, Ji J, Liu Y, Tang L (2016) Aflatoxin B₁ decontamination by UV-mutated live and immobilized Aspergillus niger. Food Control 61:235–242. https://doi.org/10.1016/j.foodcont.2015.09.017
CAS Article Google Scholar
Vilcinskas K, Zlopasa J, Jansen K, Mulder FM, Picken SJ, Koper GJ (2016) Water sorption and diffusion in (reduced) graphene oxide-alginate biopolymer nanocomposites. Macromol Mater Eng 301(9):1049–1063. https://doi.org/10.1002/mame.201600154
CAS Article Google Scholar
Wang J, Chen C (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol Adv 24(5):427–451. https://doi.org/10.1016/j.biotechadv.2006.03.001
CAS Article Google Scholar
Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27(2):195–226. https://doi.org/10.1016/j.biotechadv.2008.11.002
Article Google Scholar
Wang X, Liang X, Wang Y, Wang X, Liu M, Yin D, Xia S, Zhao J, Zhang Y (2011) Adsorption of copper (II) onto activated carbons from sewage sludge by microwave-induced phosphoric acid and zinc chloride activation. Desalination 278(1-3):231–237. https://doi.org/10.1016/j.desal.2011.05.033
CAS Article Google Scholar
Wang P, Du M, Zhu H, Bao S, Yang T, Zou M (2015) Structure regulation of silica nanotubes and their adsorption behaviors for heavy metal ions: pH effect, kinetics, isotherms and mechanism. J Hazard Mater 286:533–544. https://doi.org/10.1016/j.jhazmat.2014.12.034
CAS Article Google Scholar
Wang F, Lu X, Li XY (2016a) Selective removals of heavy metals (Pb²⁺, Cu²⁺, and Cd²⁺) from wastewater by gelation with alginate for effective metal recovery. J Hazard Mater 308:75–83. https://doi.org/10.1016/j.jhazmat.2016.01.021
CAS Article Google Scholar
Wang H, Gao H, Chen M, Xu X, Wang X, Pan C, Gao J (2016b) Microwave-assisted synthesis of reduced graphene oxide/titania nanocomposites as an adsorbent for methylene blue adsorption. Appl Surf Sci 360:840–848. https://doi.org/10.1016/j.apsusc.2015.11.075
CAS Article Google Scholar
Xu M, Hadi P, Chen G, McKay G (2014) Removal of cadmium ions from wastewater using innovative electronic waste-derived material. J Hazard Mater 273:118–123. https://doi.org/10.1016/j.jhazmat.2014.03.037
CAS Article Google Scholar
Zagrodnik R, Thiel M, Seifert K, Włodarczak M, Łaniecki M (2013) Application of immobilized Rhodobacter sphaeroides bacteria in hydrogen generation process under semi-continuous conditions. Int J Hydrogen Energy 38(18):7632–7639. https://doi.org/10.1016/j.ijhydene.2013.01.023
CAS Article Google Scholar
Zieleniewska M, Leszczyński MK, Szczepkowski L, Bryśkiewicz A, Krzyżowska M, Bień K, Ryszkowska J (2016) Development and applicational evaluation of the rigid polyurethane foam composites with egg shell waste. Polym Degrad Stab 132:78–86. https://doi.org/10.1016/j.polymdegradstab.2016.02.030
CAS Article Google Scholar

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Acknowledgements

This study was supported by the National Key Technology Research and Development Program of the Ministry of Science and Technology of China (2015BAD17B02).

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College of Food Science and Engineering, Ocean University of China, Qingdao, 266003, People’s Republic of China
Wenyu Zhao, Ting Zhou, Junxiang Zhu, Xun Sun & Ying Xu
Marine Fisheries Research Institute of Zhejiang, Zhoushan, 316021, People’s Republic of China
Junxiang Zhu

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Wenyu Zhao
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Ting Zhou
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Junxiang Zhu
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Xun Sun
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Ying Xu
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Correspondence to Ying Xu.

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Responsible editor: Guilherme L. Dotto

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Zhao, W., Zhou, T., Zhu, J. et al. Adsorption of cadmium ions using the bioadsorbent of Pichia kudriavzevii YB5 immobilized by polyurethane foam and alginate gels. Environ Sci Pollut Res 25, 3745–3755 (2018). https://doi.org/10.1007/s11356-017-0785-5

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Received: 06 October 2017
Accepted: 16 November 2017
Published: 22 November 2017
Issue Date: February 2018
DOI: https://doi.org/10.1007/s11356-017-0785-5

Keywords

P. kudriavzevii YB5
Immobilization
Polyurethane foam
Alginate gels
Cadmium ions
Bioadsorption