Abstract
Iron oxide nanoparticles (IONs) may well represent the most promising magnetic nanostructures for a plethora of applications in health, life and environmental science. IONs are already used in medicine, catalysis and downstream processing of biotechnological products. Since most particles, utilized industrially, need expensive coatings, the application of bare nanoparticles seems economically worthwhile. In this study, three different ION species were synthesized by co-precipitation methods without stabilizing agents and were thoroughly characterized with a multi-analytical approach. We emphasize the importance of the particle characterization as transitions of the ION polymorphs into each other are possible as well as merging of distinct properties. The particle sizes, which here range from 10 to 30 nm, and the magnetic properties of IONs are crucial for the further application. The adsorption behavior of the enzyme cellulase (CEL) as a model protein is investigated on the different IONs in order to gain deeper insights into bio-nano interactions to different surface sites, charges, curvatures and morphologies, as given by the three applied adsorber materials. The protein-particle interactions are driven by electrostatic and hydrophobic forces in the case of CEL. The CEL adsorption follows a Langmuir behavior and does not exceed maximum loads of around 0.6 g g−1. IR spectroscopy gives insights into the orientation of bound CEL and indicates a stronger affinity for the β-sheet tertiary structure content while a higher load can be reached with a higher α-helix content.
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References
Ahn, T., Kim, J.H., Yang, H.-M., Lee, J.W., Kim, J.-D.: Formation pathways of magnetite nanoparticles by coprecipitation method. J. Phys. Chem. C. 116(10), 6069–6076 (2012)
Albornoz, C., Jacobo, S.E.: Preparation of a biocompatible magnetic film from an aqueous ferrofluid. J. Magn. Magn. Mater. 305(1), 12–15 (2006)
Baaziz, W., Pichon, B.P., Fleutot, S., Liu, Y., Lefevre, C., Greneche, J.-M., Toumi, M., Mhiri, T., Begin-Colin, S.: Magnetic iron oxide nanoparticles: reproducible tuning of the size and nanosized-dependent composition, defects, and spin canting. J. Phys. Chem. C. 118(7), 3795–3810 (2014)
Berry, F.J., Skinner, S., Thomas, M.F.: Mössbauer spectroscopic examination of a single crystal of Fe3O4. J. Phys. 10(1), 215–220 (1998)
Bersani, D., Lottici, P.P., Montenero, A.: Micro-raman investigation of iron oxide films and powders produced by sol–gel synthesis. J. Raman Spectrosc. 30, 355–360 (1999)
Bødker, F., Mørup, S.: Size dependence of the properties of hematite nanoparticles. Europhys. Lett. 52(2), 217 (2000)
Bødker, F., Hansen, M.F., Koch, C.B., Lefmann, K., Mørup, S.: Magnetic properties of hematite nanoparticles. Phys. Rev. B. 61(10), 6826–6838 (2000)
Bornscheuer, U., Buchholz, K., Seibel, J.: Enzymatic degradation of (ligno)cellulose. Angew. Chem. Int. Ed. 53(41), 10876–10893 (2014)
Carlson, J.J., Kawatra, S.K.: Factors affecting zeta potential of iron oxides. Miner. Process. Extr. Metall. Rev. 34(5), 269–303 (2013)
Chamritski, I., Burns, G.: Infrared- and Raman-active phonons of magnetite, maghemite, and hematite: a computer simulation and spectroscopic study. J. Phys. Chem. B. 109(11), 4965–4968 (2005)
Chernyshova, I.V., Ponnurangam, S., Somasundaran, P.: On the origin of an unusual dependence of (bio)chemical reactivity of ferric hydroxides on nanoparticle size. Phys. Chem. Chem. Phys. 12(42), 14045–14056 (2010)
Colombo, M., Carregal-Romero, S., Casula, M.F., Gutiérrez, L., Morales, M.P., Böhm, I.B., Heverhagen, J.T., Prosperi, D., Parak, W.J.: Biological applications of magnetic nanoparticles. Chem. Soc. Rev. 41(11), 4306–4334 (2012)
Cornell, R.M., Schwertmann, U.: The Iron Oxides. Wiley, Weinheim (2003)
Drenkova-Tuhtan, A., Mandel, K., Paulus, A., Meyer, C., Hutter, F., Gellermann, C., Sextl, G., Franzreb, M., Steinmetz, H.: Phosphate recovery from wastewater using engineered superparamagnetic particles modified with layered double hydroxide ion exchangers. Water Res. 47(15), 5670–5677 (2013)
Fang, M., Ström, V., Olsson, R.T., Belova, L., Rao, K.V.: Particle size and magnetic properties dependence on growth temperature for rapid mixed co-precipitated magnetite nanoparticles. Nanotechnology. 23(14), 145601 (2012)
Fraga García, P., Freiherr von Roman, M., Reinlein, S., Wolf, M., Berensmeier, S.: Impact of nanoparticle aggregation on protein recovery through a pentadentate chelate ligand on magnetic carriers. ACS Appl. Mater. Interfaces. 6(16), 13607–13616 (2014)
Fraga García, P., Brammen, M., Wolf, M., Reinlein, S., Freiherr von Roman, M., Berensmeier, S.: High-gradient magnetic separation for technical scale protein recovery using low cost magnetic nanoparticles. Sep. Purif. Technol. 150, 29–36 (2015)
Franzreb, M., Siemann-Herzberg, M., Hobley, T.J., Thomas, Ow en R, T.: Protein purification using magnetic adsorbent particles. Appl. Microbiol. Biotechnol. 70(5), 505–516 (2006)
Gdula, K., Dąbrowski, A., Skwarek, E.: Synthesis, surface characterization and electrokinetic properties of colloidal silica nanoparticles with magnetic core. Adsorption 22(4–6), 681–688 (2016)
Goss, C.J.: Saturation magnetisation, coercivity and lattice parameter changes in the system Fe3O4-γFe2O3, and their relationship to structure. Phys. Chem. Miner. 16(2) (1988)
Gotić, M., Koščec, G., Musić, S.: Study of the reduction and reoxidation of substoichiometric magnetite. J. Mol. Struct. 924–926, 347–354 (2009)
Graham, D.L., Ferreira, H.A., Freitas, P.P.: Magnetoresistive-based biosensors and biochips. Trends Biotechnol. 22(9), 455–462 (2004)
Illés, E., Tombácz, E.: The role of variable surface charge and surface complexation in the adsorption of humic acid on magnetite. Colloids Surf. A 230(1–3), 99–109 (2003)
Jesionowski, T., Zdarta, J., Krajewska, B.: Enzyme immobilization by adsorption: a review. Adsorption 20(5–6), 801–821 (2014)
Jordan, J., Kumar, C.S., Theegala, C.: Preparation and characterization of cellulase-bound magnetite nanoparticles. J. Mol. Catal. B 68(2), 139–146 (2011)
Jubb, A.M., Allen, H.C.: Vibrational spectroscopic characterization of hematite, maghemite, and magnetite thin films produced by vapor deposition. ACS Appl. Mater. Interfaces. 2(10), 2804–2812 (2010)
Khajehpour, M., Dashnau, J.L., Vanderkooi, J.M.: Infrared spectroscopy used to evaluate glycosylation of proteins. Anal. Biochem. 348(1), 40–48 (2006)
Khalafalla, S., Reimers, G.W.: Magnetofluids and their manufacture. USA US3764540 A, 09.10.1973
Kim, E.H., Lee, H.S., Kwak, B.K., Kim, B.-K.: Synthesis of ferrofluid with magnetic nanoparticles by sonochemical method for MRI contrast agent. J. Magn. Magn. Mater. 289, 328–330 (2005)
Kim, W., Suh, C.-Y., Cho, S.-W., Roh, K.-M., Kwon, H., Song, K., Shon, I.-J.: A new method for the identification and quantification of magnetite-maghemite mixture using conventional X-ray diffraction technique. Talanta 94, 348–352 (2012)
Kimata, M., Nakagawa, D., Hasegawa, M.: Preparation of monodisperse magnetic particles by hydrolysis of iron alkoxide. Powder Technol. 132(2–3), 112–118 (2003)
Kolhatkar, A.G., Jamison, A.C., Litvinov, D., Willson, R.C., Lee, T.R.: Tuning the magnetic properties of nanoparticles. Int. J. Mol. Sci. 14(8), 15977–16009 (2013)
Kudina, O., Zakharchenko, A., Trotsenko, O., Tokarev, A., Ionov, L., Stoychev, G., Puretskiy, N., Pryor, S.W., Voronov, A., Minko, S.: Highly efficient phase boundary biocatalysis with enzymogel nanoparticles. Angew. Chem., Int. Ed. Engl. 53(2), 483–487 (2014)
Lee, N., Hyeon, T.: Designed synthesis of uniformly sized iron oxide nanoparticles for efficient magnetic resonance imaging contrast agents. Chem. Soc. Rev. 41(7), 2575–2589 (2012)
Li, D., Teoh, W.Y., Selomulya, C., Woodward, R.C., Amal, R., Rosche, B.: Flame-sprayed superparamagnetic bare and silica-coated maghemite nanoparticles: synthesis, characterization, and protein adsorption–desorption. Chem. Mater. 18(26), 6403–6413 (2006)
Lu, A.-H., Salabas, E.L., Schüth, F.: Magnetic nanoparticles: synthesis, protection, functionalization, and application. Angew. Chem. Int. Ed. Engl. 46(8), 1222–1244 (2007)
Massart, R.: Preparation of aqueous magnetic liquids in alkaline and acidic media. IEEE Trans. Magn. 17(2), 1247–1248 (1981)
Mikhaylov, G., Mikac, U., Magaeva, A.A., Itin, V.I., Naiden, E.P., Psakhye, I., Babes, L., Reinheckel, T., Peters, C., Zeiser, R., Bogyo, M., Turk, V., Psakhye, S.G., Turk, B., Vasiljeva, O.: Ferri-liposomes as an MRI-visible drug-delivery system for targeting tumours and their microenvironment. Nat. Nanotechnol. 6(9), 594–602 (2011)
Morhardt, C., Ketterer, B., Heißler, S., Franzreb, M.: Direct quantification of immobilized enzymes by means of FTIR ATR spectroscopy—a process analytics tool for biotransformations applying non-porous magnetic enzyme carriers. J. Mol. Catal. B 107, 55–63 (2014)
Oh, S., Cook, D.C., Townsend, H.E.: Characterization of iron oxides commonly formed as corrosion products on steel. Hyperfine Interact. 112(1–4), 59–66 (1998)
Pavlidis, I.V., Vorhaben, T., Tsoufis, T., Rudolf, P., Bornscheuer, U.T., Gournis, D., Stamatis, H.: Development of effective nanobiocatalytic systems through the immobilization of hydrolases on functionalized carbon-based nanomaterials. Bioresour. Technol. 115, 164–171 (2012)
Peng, Z.G., Hidajat, K., Uddin, M.S.: Adsorption of bovine serum albumin on nanosized magnetic particles. J. Colloid Interface Sci. 271(2), 277–283 (2004)
Rezwan, K., Meier, L.P., Rezwan, M., Voros, J., Textor, M., Gauckler, L.J.: Bovine serum albumin adsorption onto colloidal Al2O3 particles: a new model based on zeta potential and UV–vis measurements. Langmuir. 20(23), 10055–10061 (2004)
Roach, P., Farrar, D., Perry, C.C.: Interpretation of protein adsorption: surface-induced conformational changes. J. Am. Chem. Soc. 127(22), 8168–8173 (2005)
Rossi, L.M., Costa, Natalia J. S., Silva, F.P., Wojcieszak, R.: Magnetic nanomaterials in catalysis: advanced catalysts for magnetic separation and beyond. Green Chem. 16(6), 2906–2933 (2014)
Roth, H.-C., Schwaminger, S.P., Schindler, M., Wagner, F.E., Berensmeier, S.: Influencing factors in the co-precipitation process of superparamagnetic iron oxide nano particles: a model based study. J. Magn. Magn. Mater. 377, 81–89 (2015)
Roth, H.-C., Schwaminger, S., Fraga García, P., Ritscher, J., Berensmeier, S.: Oleate coating of iron oxide nanoparticles in aqueous systems: the role of temperature and surfactant concentration. J. Nanopart. Res. 18(4) (2016a)
Roth, H.-C., Schwaminger, S.P., Peng, F., Berensmeier, S.: Immobilization of cellulase on magnetic nanocarriers. ChemistryOpen 5(3), 183–187 (2016b)
Salazar-Alvarez, G., Muhammed, M., Zagorodni, A.A.: Novel flow injection synthesis of iron oxide nanoparticles with narrow size distribution. Chem. Eng Sci. 61(14), 4625–4633 (2006)
Santoyo Salazar, J., Perez, L., de Abril, O., Truong Phuoc, L., Ihiawakrim, D., Vazquez, M., Greneche, J.-M., Begin-Colin, S., Pourroy, G.: Magnetic iron oxide nanoparticles in 10–40 nm range: composition in terms of magnetite/maghemite ratio and effect on the magnetic properties. Chem. Mater. 23(6), 1379–1386 (2011)
Schultz, N., Metreveli, G., Franzreb, M., Frimmel, F.H., Syldatk, C.: Zeta potential measurement as a diagnostic tool in enzyme immobilisation. Colloids Surf., B. 66(1), 39–44 (2008)
Schwaminger, S.P., Fraga García, P., Merck, G.K., Bodensteiner, F.A., Heissler, S., Günther, S., Berensmeier, S.: Nature of interactions of amino acids with bare magnetite nanoparticles. J. Phys. Chem. C. 119(40), 23032–23041 (2015)
Serefoglou, E., Litina, K., Gournis, D., Kalogeris, E., Tzialla, A.A., Pavlidis, I.V., Stamatis, H., Maccallini, E., Lubomska, M., Rudolf, P.: Smectite clays as solid supports for immobilization of β-glucosidase: synthesis, characterization, and biochemical properties. Chem. Mater. 20(12), 4106–4115 (2008)
Situm, A., Rahman, M.A., Goldberg, S., Al-Abadleh, H.A.: Spectral characterization and surface complexation modeling of low molecular weight organics on hematite nanoparticles: Role of electrolytes in the binding mechanism. Environ. Sci. 3(4), 910–926 (2016)
Sonvico, F., Mornet, S., Vasseur, S., Dubernet, C., Jaillard, D., Degrouard, J., Hoebeke, J., Duguet, E., Colombo, P., Couvreur, P.: Folate-conjugated iron oxide nanoparticles for solid tumor targeting as potential specific magnetic hyperthermia mediators: synthesis, physicochemical characterization, and in vitro experiments. Bioconjugate Chem. 16(5), 1181–1188 (2005)
Sun, Z.-X., Su, F.-W., Forsling, W., Samskog, P.-O.: Surface characteristics of magnetite in aqueous suspension. J. Colloid Interface Sci. 197(1), 151–159 (1998)
Tejirian, A., Xu, F.: Inhibition of cellulase-catalyzed lignocellulosic hydrolysis by iron and oxidative metal ions and complexes. Appl. Environ. Microbiol. 76(23), 7673–7682 (2010)
Terris, B.D., Thomson, T.: Nanofabricated and self-assembled magnetic structures as data storage media. J. Phys. D: Appl. Phys. 38(12), R199–R222 (2005)
Tombácz, E., Illés, E., Majzik, A., Hajdú, A., Rideg, N., Szekeres, M.: Ageing in the inorganic nanoworld: example of magnetite nanoparticles in aqueous medium Croat. Chem. Acta 80(3–4), 503–515 (2007)
Vereda, F., Martin-Molina, A., Hidalgo-Alvarez, R., Quesada-Perez, M.: Specific ion effects on the electrokinetic properties of iron oxide nanoparticles: experiments and simulations. Phys. Chem. Chem. Phys. 17(26), 17069–17078 (2015)
Wan, J., Chen, X., Wang, Z., Yang, X., Qian, Y.: A soft-template-assisted hydrothermal approach to single-crystal Fe3O4 nanorods. J. Cryst. Growth 276(3–4), 571–576 (2005)
Yu, S., Peralvarez-Marin, A., Minelli, C., Faraudo, J., Roig, A., Laromaine, A.: Albumin-coated SPIONs: an experimental and theoretical evaluation of protein conformation, binding affinity and competition with serum proteins. Nanoscale 8, 14393–14405 (2016)
Acknowledgements
The authors would like to express their gratitude to Prof. Dr. Tom Nilges for his support with powder XRD (TU München) and Dr. Peter Weidler for valuable discussions (Karlsruhe Institute of Technology, Institute of Functional Interfaces, Germany). Furthermore, we would like to express our very great appreciation to Dr. Marianne Hanzlik for help with TEM measurements and Stefan Darchinger for the performance of gel electrophoresis. Moreover, we are particularly grateful for the financial support of this work by the Federal Ministry of Education and Research (Grant number 031A173A) and the Bavarian Ministry of Economic Affairs and Media, Energy and Technology (Grant number 1340/68351/3/11).
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Schwaminger, S.P., Fraga-García, P., Selbach, F. et al. Bio-nano interactions: cellulase on iron oxide nanoparticle surfaces. Adsorption 23, 281–292 (2017). https://doi.org/10.1007/s10450-016-9849-y
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DOI: https://doi.org/10.1007/s10450-016-9849-y