Biotechnology Letters

, Volume 40, Issue 2, pp 237–248 | Cite as

Magnetic immobilization of bacteria using iron oxide nanoparticles

  • Dinali Ranmadugala
  • Alireza Ebrahiminezhad
  • Merilyn Manley-Harris
  • Younes Ghasemi
  • Aydin Berenjian
Review

Abstract

Bacterial cell immobilization is a novel technique used in many areas of biosciences and biotechnology. Iron oxide nanoparticles have attracted much attention in bacterial cell immobilization due to their unique properties such as superparamagnetism, large surface area to volume ratio, biocompatibility and easy separation methodology. Adhesion is the basis behind many immobilization techniques and various types of interactions determine bacterial adhesion. Efficiency of bacterial cell immobilization using iron oxide nanoparticles (IONs) generally depends on the physicochemical properties of the IONs and surface properties of bacterial cells as well as environmental/culture conditions. Bacteria exhibit various metabolic responses upon interaction with IONs, and the potential applications of iron oxide nanoparticles in bacterial cell immobilization will be discussed in this work.

Keywords

Biodetection Biofilm control Bioprocess engineering Environmental remediation Magnetic immobilization Superparamagnetism 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Amemiya Y, Arakaki A, Staniland SS, Tanaka T, Matsunaga T (2007) Controlled formation of magnetite crystal by partial oxidation of ferrous hydroxide in the presence of recombinant magnetotactic bacterial protein Mms 6. Biomaterials 28:5381–5389CrossRefPubMedGoogle Scholar
  2. Ansari F, Grigoriev P, Libor S, Tothill IE, Ramsden JJ (2009) DBT degradation enhancement by decorating Rhodococcus erythropolis IGST8 with magnetic Fe3O4 nanoparticles. Biotechnol Bioeng 102:1505–1512CrossRefPubMedGoogle Scholar
  3. Arakha M et al (2015) Antimicrobial activity of iron oxide nanoparticle upon modulation of nanoparticle-bacteria interface. Sci Rep.  https://doi.org/10.1038/srep14813 Google Scholar
  4. Aruguete DM, Hochella MF (2010) Bacteria–nanoparticle interactions and their environmental implications. Environ Chem 7:3–9CrossRefGoogle Scholar
  5. Assa F, Jafarizadeh-Malmiri H, Ajamein H, Anarjan N, Vaghari H, Sayyar Z, Berenjian A (2016) A biotechnological perspective on the application of iron oxide nanoparticles. Nano Res 9:2203–2225CrossRefGoogle Scholar
  6. Assa F, Jafarizadeh-Malmiri H, Ajamein H, Vaghari H, Anarjan N, Ahmadi O, Berenjian A (2017) Chitosan magnetic nanoparticles for drug delivery systems. Crit Rev Biotechnol 37:492–509CrossRefPubMedGoogle Scholar
  7. Auffan M et al (2008) Relation between the redox state of iron-based nanoparticles and their cytotoxicity toward Escherichia coli. Environ Sci Technol 42:6730–6735CrossRefPubMedGoogle Scholar
  8. Azam A, Ahmed AS, Oves M, Khan MS, Habib SS, Memic A (2012) Antimicrobial activity of metal oxide nanoparticles against Gram-positive and Gram-negative bacteria: a comparative study. Int J Nanomed 7:6003–6009CrossRefGoogle Scholar
  9. Bharde A et al (2006) Extracellular biosynthesis of magnetite using fungi. Small 2:135–141CrossRefPubMedGoogle Scholar
  10. Bharde AA et al (2008) Bacteria-mediated precursor-dependent biosynthesis of superparamagnetic iron oxide and iron sulfide nanoparticles. Langmuir 24:5787–5794CrossRefPubMedGoogle Scholar
  11. Borcherding J et al (2014) Iron oxide nanoparticles induce Pseudomonas aeruginosa growth, induce biofilm formation, and inhibit antimicrobial peptide function. Environ Sci 1:123–132Google Scholar
  12. Borlido L, Azevedo A, Roque A, Aires-Barros M (2013) Magnetic separations in biotechnology. Biotechnol Adv 31:1374–1385CrossRefPubMedGoogle Scholar
  13. Caccavo F, Schamberger PC, Keiding K, Nielsen PH (1997) Role of hydrophobicity in adhesion of the dissimilatory Fe (III)-reducing bacterium Shewanella alga to amorphous Fe (III) oxide. Appl Environ Microbiol 63:3837–3843PubMedPubMedCentralGoogle Scholar
  14. Cassidy M, Lee H, Trevors J (1996) Environmental applications of immobilized microbial cells: a review. J Ind Microbiol 16:79–101CrossRefGoogle Scholar
  15. Chatterjee S, Bandyopadhyay A, Sarkar K (2011) Effect of iron oxide and gold nanoparticles on bacterial growth leading towards biological application. J Nanobiotechnol 9:1–7CrossRefGoogle Scholar
  16. Chen L, Razavi FS, Mumin A, Guo X, Sham T-K, Zhang J (2013) Multifunctional nanoparticles for rapid bacterial capture, detection, and decontamination. RSC Adv 3:2390–2397CrossRefGoogle Scholar
  17. Chua H, Wong P, Yu P, Li X (1998) The removal and recovery of copper (II) ions from wastewater by magnetite immobilized cells of Pseudomonas putida 5-X. Water Sci Technol 38:315–322Google Scholar
  18. Czaczyk K, Myszka K (2007) Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Pol J Environ Stud 16:799–806Google Scholar
  19. Dickson JS, Koohmaraie M (1989) Cell surface charge characteristics and their relationship to bacterial attachment to meat surfaces. Appl Environ Microbiol 55:832–836PubMedPubMedCentralGoogle Scholar
  20. Dunhill P (1984) Immobilizing bacteria. Cell 36:796–797CrossRefGoogle Scholar
  21. Ebrahiminezhad A, Davaran S, Rasoul-Amini S, Barar J, Moghadam M, Ghasemi Y (2012a) Synthesis, characterization and anti-Listeria monocytogenes effect of amino acid coated magnetite nanoparticles. Curr Nanosci 8:868–874CrossRefGoogle Scholar
  22. Ebrahiminezhad A, Ghasemi Y, Rasoul-Amini S, Barar J, Davaran S (2012b) Impact of amino-acid coating on the synthesis and characteristics of iron-oxide nanoparticles (IONs). Bull Korean Chem Soc 33:3957–3962CrossRefGoogle Scholar
  23. Ebrahiminezhad A, Ghasemi Y, Rasoul-Amini S, Barar J, Davaran S (2013) Preparation of novel magnetic fluorescent nanoparticles using amino acids. Colloids Surf B 102:534–539CrossRefGoogle Scholar
  24. Ebrahiminezhad A, Rasoul-Amini S, Davaran S, Barar J, Ghasemi Y (2014) Impacts of iron oxide nanoparticles on the invasion power of Listeria monocytogenes. Curr Nanosci 10:382–388CrossRefGoogle Scholar
  25. Ebrahiminezhad A, Rasoul-Amini S, Kouhpayeh A, Davaran S, Barar J, Ghasemi Y (2015a) Impacts of amine functionalized iron oxide nanoparticles on HepG2 cell line. Curr Nanosci 11:113–119CrossRefGoogle Scholar
  26. Ebrahiminezhad A, Varma V, Yang S, Ghasemi Y, Berenjian A (2015b) Synthesis and application of amine functionalized iron oxide nanoparticles on Menaquinone-7 Fermentation: a step towards process intensification. Nanomaterials 6:1–9CrossRefPubMedCentralGoogle Scholar
  27. Ebrahiminezhad A, Varma V, Yang S, Berenjian A (2016) Magnetic immobilization of Bacillus subtilis natto cells for menaquinone-7 fermentation. Appl Microbiol Biotechnol 100:173–180CrossRefPubMedGoogle Scholar
  28. Ebrahiminezhad A, Barzegar Y, Ghasemi Y, Berenjian A (2017) Green synthesis and characterization of silver nanoparticles using Alcea rosea flower extract as a new generation of antimicrobials. Chem Ind Chem Eng Q 23:31–37CrossRefGoogle Scholar
  29. El-Boubbou K, Gruden C, Huang X (2007) Magnetic glyco-nanoparticles: a unique tool for rapid pathogen detection, decontamination, and strain differentiation. J Am Chem Soc 129:13392–13393CrossRefPubMedGoogle Scholar
  30. Fletcher M (1977) The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene. Can J Microbiol 23:1–6CrossRefGoogle Scholar
  31. Fletcher M (1996) Bacterial attachment in aquatic environments : A diversity of surfaces and adhesion strategies. In: Fletcher M (ed) Bacterial adhesion: molecular and ecological diversity. Wiley, New York, pp 1–24Google Scholar
  32. Galazzo JL, Bailey JE (1990) Growing Saccharomyces cerevisiae in calcium-alginate beads induces cell alterations which accelerate glucose conversion to ethanol. Biotechnol Bioeng 36:417–426CrossRefPubMedGoogle Scholar
  33. Gao J, Li L, Ho PL, Mak GC, Gu H, Xu B (2006) Combining fluorescent probes and biofunctional magnetic nanoparticles for rapid detection of bacteria in human blood. Adv Mater 18:3145–3148CrossRefGoogle Scholar
  34. Gholami A, Rasoul-amini S, Ebrahiminezhad A, Seradj SH, Ghasemi Y (2015) Lipoamino acid coated superparamagnetic iron oxide nanoparticles concentration and time dependently enhanced growth of human hepatocarcinoma cell line (Hep-G2). J Nanomater 2015: Article No. 451405  https://doi.org/10.1155/2015/451405
  35. Gholami A, Rasoul-Amini S, Ebrahiminezhad A, Abootalebi N, Niroumand U, Ebrahimi N, Ghasemi Y (2016) Magnetic properties and antimicrobial effect of amino and lipoamino acid coated iron oxide nanoparticles. Minerva Biotecnol 28:177–186Google Scholar
  36. Gnanaprakash G, Mahadevan S, Jayakumar T, Kalyanasundaram P, Philip J, Raj B (2007) Effect of initial pH and temperature of iron salt solutions on formation of magnetite nanoparticles. Mater Chem Phys 103:168–175CrossRefGoogle Scholar
  37. Grasso D, Smets B, Strevett K, Machinist B, Van Oss C, Giese R, Wu W (1996) Impact of physiological state on surface thermodynamics and adhesion of Pseudomonas aeruginosa. Environ Sci Technol 30:3604–3608CrossRefGoogle Scholar
  38. Gu H, Ho P-L, Tsang KW, Wang L, Xu B (2003) Using biofunctional magnetic nanoparticles to capture vancomycin-resistant enterococci and other gram-positive bacteria at ultralow concentration. J Am Chem Soc 125:15702–15703CrossRefPubMedGoogle Scholar
  39. Gupta AK, Gupta M (2005a) Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles. Biomaterials 26:1565–1573CrossRefPubMedGoogle Scholar
  40. Gupta AK, Gupta M (2005b) Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26:3995–4021CrossRefPubMedGoogle Scholar
  41. Hilge-Rotmann B, Rehm H-J (1991) Relationship between fermentation capability and fatty acid composition of free and immobilized Saccharomyces cerevisiae. Appl Microbiol Biotechnol 34:502–508CrossRefGoogle Scholar
  42. Ho K-C, Tsai P-J, Lin Y-S, Chen Y-C (2004) Using biofunctionalized nanoparticles to probe pathogenic bacteria. Anal Chem 76:7162–7168CrossRefPubMedGoogle Scholar
  43. Huang Y-F, Wang Y-F, Yan X-P (2010) Amine-functionalized magnetic nanoparticles for rapid capture and removal of bacterial pathogens. Environ Sci Technol 44:7908–7913CrossRefPubMedGoogle Scholar
  44. Janot R, Guérard D (2002) One-step synthesis of maghemite nanometric powders by ball-milling. J Alloys Compd 333:302–307CrossRefGoogle Scholar
  45. Jirků V (1999) Whole cell immobilization as a means of enhancing ethanol tolerance. J Ind Microbiol Biotechnol 22:147–151CrossRefGoogle Scholar
  46. Kaittanis C, Naser SA, Perez JM (2007) One-step, nanoparticle-mediated bacterial detection with magnetic relaxation. Nano Lett 7:380–383CrossRefPubMedGoogle Scholar
  47. Kekutia S, Saneblidze L, Mikelashvili V, Markhulia J, Tatarashvili R, Daraselia D, Japaridze D (2015) A new method for the synthesis of nanoparticles for biomedical applications. Eur Chem Bull 4:33–36Google Scholar
  48. Khollam Y, Dhage S, Potdar H, Deshpande S, Bakare P, Kulkarni S, Date S (2002) Microwave hydrothermal preparation of submicron-sized spherical magnetite (Fe 3O4) powders. Mater Lett 56:571–577CrossRefGoogle Scholar
  49. Laurent S, Forge D, Port M, Roch A, Robic C, Vander Elst L, Muller RN (2008) Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev 108:2064–2110CrossRefPubMedGoogle Scholar
  50. Laurent S, Dutz S, Häfeli UO, Mahmoudi M (2011) Magnetic fluid hyperthermia: focus on superparamagnetic iron oxide nanoparticles. Adv Colloid Interface Sci 166:8–23CrossRefPubMedGoogle Scholar
  51. Lee Y, Lee J, Bae CJ, Park JG, Noh HJ, Park JH, Hyeon T (2005) Large-scale synthesis of uniform and crystalline magnetite nanoparticles using reverse micelles as nanoreactors under reflux conditions. Adv Funct Mater 15:503–509CrossRefGoogle Scholar
  52. Lee C, Kim JY, Lee WI, Nelson KL, Yoon J, Sedlak DL (2008) Bactericidal effect of zero-valent iron nanoparticles on Escherichia coli. Environ Sci Technol 42:4927–4933CrossRefPubMedPubMedCentralGoogle Scholar
  53. Li Q, Mahendra S, Lyon DY, Brunet L, Liga MV, Li D, Alvarez PJ (2008) Antimicrobial nanomaterials for water disinfection and microbial control: potential applications and implications. Water Res 42:4591–4602CrossRefPubMedGoogle Scholar
  54. Li Y-G, Gao H-S, Li W-L, Xing J-M, Liu H-Z (2009) In situ magnetic separation and immobilization of dibenzothiophene-desulfurizing bacteria. Bioresour Technol 100:5092–5096CrossRefPubMedGoogle Scholar
  55. MacRae I (1985) Removal of pesticides in water by microbial cells adsorbed to magnetite. Water Res 19:825–830CrossRefGoogle Scholar
  56. MacRae I (1986) Removal of chlorinated hydrocarbons from water and wastewater by bacterial cells adsorbed to magnetite. Water Res 20:1149–1152CrossRefGoogle Scholar
  57. MacRae I, Evans SK (1983) Factors influencing the adsorption of bacteria to magnetite in water and wastewater. Water Res 17:271–277CrossRefGoogle Scholar
  58. Mahmoudi M, Sant S, Wang B, Laurent S, Sen T (2011) Superparamagnetic iron oxide nanoparticles (SPIONs): development, surface modification and applications in chemotherapy. Adv Drug Deliv Rev 63:24–46CrossRefPubMedGoogle Scholar
  59. Martelli S et al (2000) Production of iron-oxide nanoparticles by laser-induced pyrolysis of gaseous precursors. Appl Surf Sci 154:353–359CrossRefGoogle Scholar
  60. Martins SCS, Martins CM, Fiúza LMCG, Santaella ST (2013) Immobilization of microbial cells: a promising tool for treatment of toxic pollutants in industrial wastewater. Afr J Biotechnol 12:4412–4418CrossRefGoogle Scholar
  61. McEldowney S, Fletcher M (1986a) Effect of growth conditions and surface characteristics of aquatic bacteria on their attachment to solid surfaces. Microbiology 132:513–523CrossRefGoogle Scholar
  62. McEldowney S, Fletcher M (1986b) Variability of the influence of physicochemical factors affecting bacterial adhesion to polystyrene substrata. Appl Environ Microbiol 52:460–465PubMedPubMedCentralGoogle Scholar
  63. Miller M, Prinz G, Cheng S-F, Bounnak S (2002) Detection of a micron-sized magnetic sphere using a ring-shaped anisotropic magnetoresistance-based sensor: a model for a magnetoresistance-based biosensor. Appl Phys Lett 81:2211–2213CrossRefGoogle Scholar
  64. Neuberger T, Schöpf B, Hofmann H, Hofmann M, Von Rechenberg B (2005) Superparamagnetic nanoparticles for biomedical applications: possibilities and limitations of a new drug delivery system. J Magn Magn Mater 293:483–496CrossRefGoogle Scholar
  65. Pal S, Alocilja EC (2009) Electrically active polyaniline coated magnetic (EAPM) nanoparticle as novel transducer in biosensor for detection of Bacillus anthracis spores in food samples. Biosens Bioelectron 24:1437–1444CrossRefPubMedGoogle Scholar
  66. Pascal C, Pascal J, Favier F, Elidrissi Moubtassim M, Payen C (1999) Electrochemical synthesis for the control of γ-Fe2O3 nanoparticle size. Morphology, microstructure, and magnetic behavior. Chem Mater 11:141–147CrossRefGoogle Scholar
  67. Philipse AP, Maas D (2002) Magnetic colloids from magnetotactic bacteria: chain formation and colloidal stability. Langmuir 18:9977–9984CrossRefGoogle Scholar
  68. Prozorov T et al (2007) Protein-mediated synthesis of uniform superparamagnetic magnetite nanocrystals. Adv Funct Mater 17:951–957CrossRefGoogle Scholar
  69. Ranmadugala D, Ebrahiminezhad A, Manley-Harris M, Ghasemi Y, Berenjian A (2017a) The effect of iron oxide nanoparticles on Bacillus subtilis biofilm, growth and viability. Process Biochem.  https://doi.org/10.1016/j.procbio.2017.07.003 (In press)Google Scholar
  70. Ranmadugala D, Ebrahiminezhad A, Manley-Harris M, Ghasemi Y, Berenjian A (2017b) Iron oxide nanoparticles in modern microbiology and biotechnology. Crit Rev Microbiol 43:493–507CrossRefGoogle Scholar
  71. Ravindranath SP, Mauer LJ, Deb-Roy C, Irudayaraj J (2009) Biofunctionalized magnetic nanoparticle integrated mid-infrared pathogen sensor for food matrixes. Anal Chem 81:2840–2846CrossRefPubMedGoogle Scholar
  72. Rijnaarts HH, Norde W, Bouwer EJ, Lyklema J, Zehnder AJ (1995a) Reversibility and mechanism of bacterial adhesion. Colloids Surf B 4:5–22CrossRefGoogle Scholar
  73. Rijnaarts HH, Norde W, Lyklema J, Zehnder AJ (1995b) The isoelectric point of bacteria as an indicator for the presence of cell surface polymers that inhibit adhesion. Colloids Surf B 4:191–197CrossRefGoogle Scholar
  74. Rishton S et al (1997) Magnetic tunnel junctions fabricated at tenth-micron dimensions by electron beam lithography. Microelectron Eng 35:249–252CrossRefGoogle Scholar
  75. Safarik I, Safarikova M (2007) Magnetically modified microbial cells: a new type of magnetic adsorbents. China Particuol 5:19–25CrossRefGoogle Scholar
  76. Sasaki T, Terauchi S, Koshizaki N, Umehara H (1998) The preparation of iron complex oxide nanoparticles by pulsed-laser ablation. Appl Surf Sci 127:398–402CrossRefGoogle Scholar
  77. Shan G, Xing J, Zhang H, Liu H (2005) Biodesulfurization of dibenzothiophene by microbial cells coated with magnetite nanoparticles. Appl Environ Microbiol 71:4497–4502CrossRefPubMedPubMedCentralGoogle Scholar
  78. Singh N, Jenkins GJ, Asadi R, Doak SH (2010) Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev Exp 1:5358.  https://doi.org/10.3402/nano.v1i0.5358 CrossRefGoogle Scholar
  79. Singh S, Barick K, Bahadur D (2011) Surface engineered magnetic nanoparticles for removal of toxic metal ions and bacterial pathogens. J Hazard Mater 192:1539–1547CrossRefPubMedGoogle Scholar
  80. Stenström T-A, Kjelleberg S (1985) Fimbriae mediated nonspecific adhesion of Salmonella typhimurium to mineral particles. Arch Microbiol 143:6–10CrossRefPubMedGoogle Scholar
  81. Sun S, Zeng H (2002) Size-controlled synthesis of magnetite nanoparticles. J Am Chem Soc 124:8204–8205CrossRefPubMedGoogle Scholar
  82. Tartaj P, Gonzalez-Carreno T, Serna CJ (2001) Single-step nanoengineering of silica coated maghemite hollow spheres with tunable magnetic properties. Adv Mater 13:1620–1624CrossRefGoogle Scholar
  83. Tiberto P et al (2013) Magnetic properties of jet-printer inks containing dispersed magnetite nanoparticles. Eur Phys J B 86:1–6CrossRefGoogle Scholar
  84. Touhami A, Jericho MH, Boyd JM, Beveridge TJ (2006) Nanoscale characterization and determination of adhesion forces of Pseudomonas aeruginosa pili by using atomic force microscopy. J Bacteriol 188:370–377CrossRefPubMedPubMedCentralGoogle Scholar
  85. Tsuneda S, Aikawa H, Hayashi H, Yuasa A, Hirata A (2003) Extracellular polymeric substances responsible for bacterial adhesion onto solid surface. FEMS Microbiol Lett 223:287–292CrossRefPubMedGoogle Scholar
  86. Vaghari H, Eskandari M, Sobhani V, Berenjian A, Song Y, Jafarizadeh-Malmiri H (2015) Process intensification for production and recovery of biological products. Am J Biochem Biotechnol 11:37–43CrossRefGoogle Scholar
  87. Vaghari H, Jafarizadeh-Malmiri H, Mohammadlou M, Berenjian A, Anarjan N, Jafari N, Nasiri S (2016) Application of magnetic nanoparticles in smart enzyme immobilization. Biotechnol Lett 38:223–233CrossRefPubMedGoogle Scholar
  88. Van Iersel M, Brouwer-Post E, Rombouts F, Abee T (2000) Influence of yeast immobilization on fermentation and aldehyde reduction during the production of alcohol-free beer. Enzyme Microb Technol 26:602–607CrossRefPubMedGoogle Scholar
  89. Verma A, Stellacci F (2010) Effect of surface properties on nanoparticle–cell interactions. Small 6:12–21CrossRefPubMedGoogle Scholar
  90. Vijayakumar R, Koltypin Y, Felner I, Gedanken A (2000) Sonochemical synthesis and characterization of pure nanometer-sized Fe3O4 particles. Mater Sci Eng, A 286:101–105CrossRefGoogle Scholar
  91. Wang Y, Ravindranath S, Irudayaraj J (2011) Separation and detection of multiple pathogens in a food matrix by magnetic SERS nanoprobes. Anal Bioanal Chem 399:1271–1278CrossRefPubMedGoogle Scholar
  92. Weinstein JS et al (2010) Superparamagnetic iron oxide nanoparticles: diagnostic magnetic resonance imaging and potential therapeutic applications in neurooncology and central nervous system inflammatory pathologies, a review. J Cereb Blood Flow Metab 30:15–35CrossRefPubMedGoogle Scholar
  93. Wiesner MR, Lowry GV, Alvarez P, Dionysiou D, Biswas P (2006) Assessing the risks of manufactured nanomaterials. Environ Sci Technol 40:4336–4345CrossRefPubMedGoogle Scholar
  94. Wu W, He Q, Jiang C (2008) Magnetic iron oxide nanoparticles: synthesis and surface functionalization strategies. Nanoscale Res Lett 3:397–415CrossRefPubMedPubMedCentralGoogle Scholar
  95. Zhang D, Tong Z, Li S, Zhang X, Ying A (2008) Fabrication and characterization of hollow Fe3O4 nanospheres in a microemulsion. Mater Lett 62:4053–4055CrossRefGoogle Scholar
  96. Zhao X, Hilliard LR, Mechery SJ, Wang Y, Bagwe RP, Jin S, Tan W (2004) A rapid bioassay for single bacterial cell quantitation using bioconjugated nanoparticles. PNAS 101:15027–15032CrossRefPubMedPubMedCentralGoogle Scholar
  97. Zucca P, Sanjust E (2014) Inorganic materials as supports for covalent enzyme immobilization: methods and mechanisms. Molecules 19:14139–14194CrossRefPubMedGoogle Scholar
  98. Żur J, Wojcieszyńska D, Guzik U (2016) Metabolic Responses of Bacterial Cells to Immobilization. Molecules 21: Article Number: UNSP 958  https://doi.org/10.3390/molecules21070958

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Dinali Ranmadugala
    • 1
  • Alireza Ebrahiminezhad
    • 2
    • 3
  • Merilyn Manley-Harris
    • 1
  • Younes Ghasemi
    • 3
  • Aydin Berenjian
    • 1
  1. 1.Faculty of Science & EngineeringUniversity of WaikatoHamiltonNew Zealand
  2. 2.Department of Medical Biotechnology, School of Medicine, and Noncommunicable Diseases Research CentreFasa University of Medical SciencesFasaIran
  3. 3.Pharmaceutical Sciences Research CenterShiraz University of Medical SciencesShirazIran

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