This paper is published as part of a PCCP Themed Issue on: Metal oxide nanostructures: synthesis, properties and applications

Guest Editors: Nicola Pinna, Markus Niederberger, John Martin Gregg and Jean-Francois Hochepied

Editorial Chemistry and physics of metal oxide nanostructures Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b905768d

Papers Thermally stable ordered mesoporous CeO2/TiO2 visible-light photocatalysts Guisheng Li, Dieqing Zhang and Jimmy C. Yu, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b819167k Blue nano titania made in diffusion flames Alexandra Teleki and Sotiris E. Pratsinis, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821590a Shape control of iron oxide nanoparticles Alexey Shavel and Luis M. Liz-Marzán, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b822733k Colloidal semiconductor/magnetic heterostructures based on iron-oxide-functionalized brookite TiO2 nanorods Raffaella Buonsanti, Etienne Snoeck, Cinzia Giannini, Fabia Gozzo, Mar Garcia-Hernandez, Miguel Angel Garcia, Roberto Cingolani and Pantaleo Davide Cozzoli, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821964h Low-temperature ZnO atomic layer deposition on biotemplates: flexible photocatalytic ZnO structures from eggshell membranes Seung-Mo Lee, Gregor Grass, Gyeong-Man Kim, Christian Dresbach, Lianbing Zhang, Ulrich Gösele and Mato Knez, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b820436e A LEEM/ -LEED investigation of phase transformations in TiOx/Pt(111) ultrathin films Stefano Agnoli, T. Onur Mente , Miguel A. Niño, Andrea Locatelli and Gaetano Granozzi, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821339a Synthesis and characterization of V2O3 nanorods Alexander C. Santulli, Wenqian Xu, John B. Parise, Liusuo Wu, M.C. Aronson, Fen Zhang, Chang-Yong Nam, Charles T. Black, Amanda L. Tiano and Stanislaus S. Wong, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b822902c

Flame spray-pyrolyzed vanadium oxide nanoparticles for lithium battery cathodes See-How Ng, Timothy J. Patey, Robert Büchel, Frank Krumeich, Jia-Zhao Wang, Hua-Kun Liu, Sotiris E. Pratsinis and Petr Novák, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821389p Mesoporous sandwiches: towards mesoporous multilayer films of crystalline metal oxides Rainer Ostermann, Sébastien Sallard and Bernd M. Smarsly, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b820651c Surprisingly high, bulk liquid-like mobility of silica-confined ionic liquids Ronald Göbel, Peter Hesemann, Jens Weber, Eléonore Möller, Alwin Friedrich, Sabine Beuermann and Andreas Taubert, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821833a Fabrication of highly ordered, macroporous Na2W4O13 arrays by spray pyrolysis using polystyrene colloidal crystals as templates SunHyung Lee, Katsuya Teshima, Maki Fujisawa, Syuji Fujii, Morinobu Endo and Shuji Oishi, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821209k Nanoporous Ni–Ce0.8Gd0.2O1.9-x thin film cermet SOFC anodes prepared by pulsed laser deposition Anna Infortuna, Ashley S. Harvey, Ulrich P. Muecke and Ludwig J. Gauckler, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821473e Surface chemistry of carbon-templated mesoporous aluminas Thomas Onfroy, Wen-Cui Li, Ferdi Schüth and Helmut Knözinger, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821505g ZnO@Co hybrid nanotube arrays growth from electrochemical deposition: structural, optical, photocatalytic and magnetic properties Li-Yuan Fan and Shu-Hong Yu, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b823379a Electrochemistry of LiMn2O4 nanoparticles made by flame spray pyrolysis T. J. Patey, R. Büchel, M. Nakayama and P. Novák, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821572n Ligand dynamics on the surface of zirconium oxo clusters Philip Walther, Michael Puchberger, F. Rene Kogler, Karlheinz Schwarz and Ulrich Schubert, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b820731c

Thin-walled Er3+:Y2O3 nanotubes showing up-converted fluorescence Christoph Erk, Sofia Martin Caba, Holger Lange, Stefan Werner, Christian Thomsen, Martin Steinhart, Andreas Berger and Sabine Schlecht, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821304f Wettability conversion of colloidal TiO2 nanocrystal thin films with UV-switchable hydrophilicity Gianvito Caputo, Roberto Cingolani, Pantaleo Davide Cozzoli and Athanassia Athanassiou, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b823331d Nucleation and growth of atomic layer deposition of HfO2 gate dielectric layers on silicon oxide: a multiscale modelling investigation A. Dkhissi, G. Mazaleyrat, A. Estève and M. Djafari Rouhani, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821502b Designing meso- and macropore architectures in hybrid organic–inorganic membranes by combining surfactant and breath figure templating (BFT) Ozlem Sel, Christel Laberty-Robert, Thierry Azais and Clément

Sanchez, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821506e The controlled deposition of metal oxides onto carbon nanotubes by atomic layer deposition: examples and a case study on the application of V2O4 coated nanotubes in gas sensing Marc-Georg Willinger, Giovanni Neri, Anna Bonavita, Giuseppe Micali, Erwan Rauwel, Tobias Herntrich and Nicola Pinna, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821555c In situ investigation of molecular kinetics and particle formation of water-dispersible titania nanocrystals G. Garnweitner and C. Grote, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b821973g Chemoresistive sensing of light alkanes with SnO2 nanocrystals: a DFT-based insight Mauro Epifani, J. Daniel Prades, Elisabetta Comini, Albert Cirera, Pietro Siciliano, Guido Faglia and Joan R. Morante, Phys. Chem. Chem. Phys., 2009 DOI: 10.1039/b820665a

PAPER

www.rsc.org/pccp | Physical Chemistry Chemical Physics

Low-temperature ZnO atomic layer deposition on biotemplates: flexible photocatalytic ZnO structures from eggshell membranes Seung-Mo Lee,*a Gregor Grass,b Gyeong-Man Kim,c Christian Dresbach,d Lianbing Zhang,a Ulrich Go¨selea and Mato Knez*a Received 17th November 2008, Accepted 5th February 2009 First published as an Advance Article on the web 6th March 2009 DOI: 10.1039/b820436e Macroporous ZnO membranes with a strong photocatalytic effect and high mechanical flexibility were prepared from inner shell membranes (ISM) of avian eggshells as templates after performing low-temperature ZnO atomic layer deposition (ALD). In order to evaluate the potential merits and general applicability of the ZnO structures, a comparative study of two membranes with coatings of either TiO2 or ZnO, processed under similar conditions, was performed. The study includes crystallographic features, mechanical and thermal stability and bactericidal efficiency. Both, the ZnO and the TiO2 coated membranes clearly exhibited bactericidal effects as well as mechanical flexibility and thermal stability even at relatively high temperatures. The ZnO membranes, even though prepared at fairly low temperatures (B100 1C), exhibited polycrystalline phases and showed a good bactericidal efficiency as well as higher mechanical flexibility than the TiO2 coated membranes. This study shows the benefits of low-temperature ZnO ALD i.e., the thermally non-destructive nature, which preserves the mechanical stability and the native morphology of the templates used, together with an added functionality, i.e. the bactericidal effect.

1. Introduction During the evolution of biological creatures, numerous microand nanostructures with specific functionalities developed for adaptation to environmental conditions. Adoption of such structures by mimicking or templating came into focus of science in recent years.1 Functionalization of structures by coating biological templates is one of the methods to produce more stable organic or inorganic micro/nanostructures. So far those coatings have been performed mainly by chemical vapor deposition and sol-gel strategies on various biotemplates such as cellulose,2 wool,3 butterfly wings,4 superhydrophobic plant leaves4 and pine wood.5 However, these methods have some limitations in processing, such as occasional non-uniform coating of large templates or demanding film thickness control.6,7 As a promising method to overcome these processing limitations, atomic layer deposition (ALD) has recently attracted attention. Advantages of ALD are the conformal replication of 3D morphologies, large area uniformity, precise film thickness control on the nanometer scale and a wide range of operation temperatures.8–10 The feasibility of ALD for biological templates,11–13 as well as for organic materials14–16 has already been proven. However, to the best of our a

Max Planck Institute of Microstructure Physics, D-06120, Halle, Germany. E-mail: [email protected], [email protected]; Fax: +49 345 5511 223; Tel: +49 345 5582 919 b School of Biological Sciences, University of Nebraska-Lincoln, 1901 Vine Street, Lincoln, NE 68588, U. S. A. c Fraunhofer Institute for Cell Therapy and Immunology, Perlickerstraße 1, D-04103, Leipzig, Germany d Fraunhofer Institute for Mechanics of Materials, Walter-Hu¨lse-Straße 1, D-06120, Halle, Germany

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knowledge, so far ALD researchers have mainly focused their interest on the perfect coating of the fine structures of biotemplates with functional metal oxides such as TiO211 and Al2O3.11–13 Research, focusing on the optimal combination of the original functionality of the biotemplate itself and an appropriate metal oxide which can maximize additional functions of the resulting templated structures, has rarely been undertaken. Moreover, mechanical stability as a guarantee for easy handling and practical use has hardly been considered. Here, we present an example which satisfies the above requirements. As an example for a temperature sensitive biotemplate an avian eggshell membrane (ESM, Fig. 1) was processed. Those membranes were already previously used as templates for sol-gel17–19 or further deposition methods.20–22 In our studies we used the macroporous inner shell membrane (ISM) which is a part of an avian ESM (Fig. 1). It prevents bacterial invasions, thus protecting the embryo.23–25 We deposited TiO2 or ZnO by ALD on this ISM, both of which show bactericidal photocatalytic effects under UV illumination (ISM/TiO2 and ISM/ZnO).26,27 We investigated the bactericidal properties of those membranes and characterized them quantitatively using a photocatalytic reaction which inactivated Escherichia coli (E. coli) bacteria. Both resulting membranes showed successful photocatalytic functionalization of the original ISM structure in line with good bactericidal effects. ZnO membranes, even though prepared at fairly low temperatures (B100 1C), showed polycrystalline phases and exhibited stronger bactericidal effects than TiO2 coated membranes. In addition, an improved mechanical stability of the ZnO coated membranes was observed. This journal is

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Fig. 1 Structure of an avian egg and scanning electron micrographs of an inner shell membrane (ISM) of a hen’s eggshell membrane (ESM). (a) Details of an avian egg (redrawn from ref. 23) and photograph of the ISM from ESM around the air cell of the egg. (b) Low magnification SEM of an ISM viewing from the direction of the blue arrow shown in (a). (c) Magnification of several ISM fibers, showing their highly interwoven and conglutinate feature.

3. Experimental 3.1 Preparation of the inner shell membrane (ISM) from a hen’s egg Hen’s eggs were purchased from a grocery store. They were gently broken and the ISM around their air cell portion23 was carefully cut out and collected (Fig. 1a). The ISM was washed several times with deionized water in order to thoroughly remove the thin albumin layer, and were subsequently dried at room temperature for 4 h. 3.2

TiO2/ZnO atomic layer deposition (ALD) on ISM

The prepared ISM was placed in the ALD chamber (Savannah 100, Cambridge Nanotech) and dried at 70 1C for 20 min in vacuum (1  10 2 torr) with a steady Ar stream (20 sccm). For the TiO2/ZnO deposition, well established ALD processes were applied. Titanium(IV) isopropoxide (Ti(OiPr)4, TIP) and water11,28 and diethylzinc (ZnEt2, DEZ) and water29,30 were used as precursors, respectively. The Ti(OiPr)4 and ZnEt2 were purchased from Sigma Aldrich. Each cycle was composed of a pulse, exposure and purge sequence for each precursor. For the TiO2 deposition, for example, the TIP vapor was injected into the ALD chamber for 1.5 s (PULSE). Subsequently, the substrate was exposed to the TIP vapor for 30 s (EXPOSURE). The excess TIP was purged from the This journal is

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ALD chamber for 30 s (PURGE). In the same manner, the PULSE (1.3 s)/EXPOSURE (30 s)/PURGE (30 s) processes of H2O were repeated. The thickness of the TiO2 and ZnO films was adjusted by the number of cycles to 30 and 55 nm, respectively. For the preparation of diverse samples of TiO2 and ZnO, the substrate temperature was varied between 70 and 300 1C. More detailed information on the applied ALD processes and sample denotations is given in Table 1. 3.3 Characterization Scanning electron microscopy (SEM) and transmission electron microscopy (TEM) were applied to investigate the size and morphology of the samples. The investigations were conducted using a JSM-6340F at 15 kV (SEM) and JEOL 2010 at 200 kV (TEM), respectively. The crystallographic features of the metal oxide membranes were investigated by X-ray diffraction (XRD, Philips X’Pert MRD) with Cu Ka (l = 1.5421 A˚) radiation. The transfer of the samples was done in air. For y 2y measurements the samples were suspended on a silicon wafer as a convenient substrate. 3.4 Microbiology As a test strain for all bactericidal effect studies, Escherichia coli (E. coli) strain W311031 was used. A single colony was inoculated from a Luria-Bertani (LB) agar plate (Carl Roth Phys. Chem. Chem. Phys., 2009, 11, 3608–3614 | 3609

Table 1

Detailed processing conditions of the ALD process and sample denotation

Material

Precursor

Pulse/s

Exposure/s

TiO2

Ti [OCH(CH3)2]4

1.5

30

30

H2O

1.3

30

30

(C2H5)2Zn

0.1

5

15

H2O

1.5

15

150

ZnO

Purge/s

GmbH, Germany) with 4 ml of LB broth (Carl Roth GmbH, Germany) in a 10 ml glass bottle. The bottle was incubated overnight at 30 1C on an orbital shaker at 250 rpm (E. coli solution 1). After 16 h, the culture was diluted to 1 : 50 into fresh LB broth and incubated for 3 h at 250 rpm to obtain a logarithmic growing culture for bactericidal effect experiments (E. coli solution 2). The cell concentration of the E. coli solution 2 was determined by the spread plate method.32 The initial logarithmic growth phase population of E. coli ranged approximately from 105 to 106 colony forming units (CFU)/ml. 3.5

Photocatalytic experiments of ISM/TiO2 and ISM/ZnO

A reactor for the photocatalysis experiments was designed (Fig. 2). The E. coli suspension was exposed to UV light (Osram UVC-LPS 9, peak: 365 nm, power: 2W, UV light including visible blue light) from the lower part of the reactor and was continuously shaken at 250 rpm during each experiment. A 4 ml portion of E. coli solution was taken from the prepared stock solution and pippetted carefully into the reactor. The photocatalytic inactivation of the E. coli cells was assessed by taking a 100 ml volume of the E. coli solution 2 from the

Fig. 2 Schematics of the reactor for Escherichia coli (E. coli) photocatlysis experiments. The whole body was made from PTFE (polytetrafluorethylene). The sterilization was performed at high temperatures for each experiment. In order to reduce the UV absorption through the supporting part as well as to support the ISM, a PMMA (polymethyl methacrylate) sheet (1 mm thick) was used. Through the ring shaped gasket and the mechanical clamping (spring and bolt/nut type) the leakage of E. coli solution was effectively prevented.

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Cycle

Substrate temperature/1C

Sample numbering

500

70 160 225 275 300 70 100 125 200

ISM/TiO2/70 ISM/TiO2/160 ISM/TiO2/225 ISM/TiO2/275 ISM/TiO2/300 ISM/ZnO/70 ISM/ZnO/100 ISM/ZnO/125 ISM/ZnO/200

500

reactor every 5 min or 15 min for 60 min and diluting the solution 1/100 (E. coli solution 3) and 1/1000 (E. coli solution 4) with fresh LB liquid medium. In order to count the number of viable E. coli, a 10 ml volume of the E. coli solution 4 was taken and spread onto LB agar plates as described in the previous section. The thus prepared LB agar plates were incubated overnight at 37 1C. After 12 h, the number of colonies was counted. For each experiment, three plates were used and averaged. The results were plotted as the survival ratio. 3.6 Tensile test of native ISM, ISM/ZnO/100 and ISM/TiO2/275 membranes For the measurement of engineering stress (s)-engineering strain (e) behavior of the prepared samples, all ISM samples were cut with a knife (BAYHAs, Blades, No.24) to 2 mm  10B20 mm. Tensile tests were performed on a ZWICK 1445 tensile test machine with a 10 N HBM load cell, controlled by a PC with automated testing software. The extension rate was 50% of the initial testing length (10 mm) per minute (5 mm min 1). The temperature and relative humidity were 26–28 1C and 20–22%, respectively. SEM and optical microscopy (Leitz Aristomet) were used to measure the cross section area of the specimen. The thickness of the membrane was B100 mm and the width B2000 mm. Since the thickness of the ESM was not perfectly uniform, it was averaged to a yield of 100 mm from measurements at more than 20 points along the horizontal direction of each sample (2000 mm). After the tensile tests, the cross section of the fracture surface of each sample was again investigated by SEM. Because of the slightly stretched length of the sample, the cross section was slightly shrunk. However, the difference was almost negligible. In the case of the width of each sample, a similar procedure was applied. The variation in width was also negligible. For each set of data, more than 10 samples were prepared and measured at identical conditions. Each data set showed similar stress–strain behavior. As an average, from each measurement one typical data set was selected. All graphic work including data rescaling was performed with ORIGINs 7.5.

4. Results and discussion 4.1 Film quality, crystallographic features and bactericidal efficiency Since the crystallinity of the deposited coating is temperature dependent,28,33 the composite membranes were prepared at various temperatures ranging from 70 to 300 1C. The resulting This journal is

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membranes, both ISM/ZnO and ISM/TiO2, show unchanged morphological features of the original ISM. As representative SEM and TEM micrographs of the resulting ISM/ZnO and ISM/TiO2 membranes, the images of ISM/ZnO/100 and ISM/TiO2/275 are shown in Fig. 3 (sample denotations can be found in Table 1; the reason that we choose these two samples as representative samples will be discussed in a further section). Both images show, as expected, good quality of the metal oxide deposition. The films were conformally deposited over the whole collagen membrane without any distortion and shrinkage, as can be confirmed from Fig. 3a, c and e showing fibers of ISM/ZnO/100 and Fig. 3b, d and f showing fibers of ISM/TiO2/275. Apart from the deposited film quality, the bactericidal properties, as a function of the crystallographic features of the resulting macroporous membranes, are of interest. Fig. 4a and b show X-ray diffraction (XRD) patterns of the ISM/TiO2

Table 2 Maximum stress (MPa) and strain (%) value of Native ISM, ISM/TiO2/275 and ISM/ZnO/100 (Average  standard deviation)

Native ISM ISM/TiO2/275 ISM/ZnO/100

Maximum stress (smax)/MPa

Maximum strain (emax)/%

6.21  0.62 6.02  0.25 9.09  0.71

6.18  0.52 3.45  0.43 9.02  0.83

and ISM/ZnO prepared at temperatures ranging from 70 to 300 1C. The TiO2-coated membranes (ISM/TiO2) processed at 70 and 160 1C did not show any obvious diffraction peaks, whereas in the higher temperature range they showed reflections from the anatase phase (ICDD card No. 21-1272), anatase (101) being the strongest peak among them. The deposition temperature of 225 1C shows an onset of crystallization. In

Fig. 3 Electron micrographs of ISM/ZnO/100 and ISM/TiO2/275. Parts (a) and (b) display a macroscopic view of the ISM/ZnO/100 and the ISM/TiO2/275 membrane, respectively, showing the morphology of the native ISM (their highly interwoven and conglutinate feature). Parts (c) and (d) show the composite membranes of collagen fibers/metal oxides at high magnification. Parts (e) and (f) display the corresponding transmission electron microscope (TEM) images of the ISM/ZnO/100 and ISM/TiO2/275 membrane, respectively, showing the coating of the fibers with the metal oxide.

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Fig. 4 X-Ray diffraction (XRD) patterns and E. coli survival curves related to ISM/TiO2 (upper row) and ISM/ZnO (lower row). (a) and (b) XRD patterns of both membranes illustrating the effect of the deposition temperature. (c) and (d) E. coli survival curves in aqueous solution over time corresponding to each membrane after the UV illumination for various deposition temperatures of TiO2 and ZnO, respectively.

contrast, the ZnO coated membranes (ISM/ZnO) showed diffraction peaks already after the 70 1C ALD deposition process. The positions and the intensities of the individual peaks are in good agreement with the hexagonal wurtzite structure of ZnO according to JCPDS card No. 36-1451. The photocatalytic efficiency (bactericidal effect) was evaluated from the E. coli survival ratio with respect to the illumination time with UV light for the two different types of metal oxide membranes. It is generally known that semiconducting metal oxides, such as ZnO and TiO2 generate conduction electrons (e ) and valence band holes (h+) on the surface upon illumination with an energy higher than the band gap energy (Eg,ZnO = 3.37 eV, Eg,TiO2 = 3.2 eV) in an aqueous solution.26,27 Subsequently, holes react with the water adhering to the surface of the ZnO and TiO2 to form highly reactive hydroxyl radicals (OH ). Oxygen acts as an electron acceptor forming super-oxide radical anions (O2 ) which are an additional source of hydroxyl radicals upon subsequent 3612 | Phys. Chem. Chem. Phys., 2009, 11, 3608–3614

formation of hydrogen peroxide (H2O2).26,27 The generated OH , O2 and H2O2 can attack the cell walls in E. coli, which will finally be damaged. After eliminating the protection of the cell wall, oxidation of the underlying cystoplasmic membrane and the intracellular contents takes place and eventually leads to the death of the E. coli.34 As illustrated in Fig. 4c and d, in the dark without ZnO and TiO2, the survival ratio was constant or slightly increased due to the natural replication of the E. coli. Under UV illumination both membranes clearly showed the capability to inactivate E. coli in aqueous solution. In agreement with previous literature, it was observed that the bactericidal effect of ZnO and TiO2 has a stronger dependence on the crystallinity than on the film thickness.35,36 Specifically, the bactericidal efficiency of the ISM/TiO2 with anatase/rutile phases and the ISM/ZnO with the hexagonal phase revealed a proportional relationship to the ALD deposition temperature and the relative intensity of the (100) crystal direction, respectively. This journal is

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The membrane itself has a strong impact on photocatalytic behavior. From the respective E. coli survival curve, it can be seen that, in terms of bactericidal efficiency under UV illumination, the ISM without metal oxide coating is more effective than just the suspension only, i.e. without a membrane. The metal oxide coating enhances the efficiency drastically. Comparing the bactericidal efficiency of the coated membranes with TiO2 particles (Degussa P25, average particle size: 30 nm)37 or home-made TiO2 films38 reported in the literature, the ISM/TiO2/300 is much more efficient when considering the irradiation intensity and the area exposed to UV light. Similar to TiO2, the ISM/ZnO/100 also shows higher efficiency, as compared to ZnO powder39,40 with a much lager surface area. Presumably, this is caused by the macroporous structure of the ISM. Probably, E. coli bacteria can easily adhere to the macroporous ISM, leading to an increased concentration of bacteria close to the UV source. Thus more bacteria are destroyed in the same time period. It is noteworthy that ISM/TiO2 reveals a higher bactericidal efficiency than ISM/ZnO. This result is consistent with a previous publication comparing the photocatalytic efficiency of TiO2 and ZnO,41 however, opposite results have also been reported.42,43 The relative photocatalytic behavior of TiO2 and ZnO still seems to be ambiguous. The graphs in Fig. 4c and d show that, as expected, ISM/TiO2/300 has the strongest bactericidal effects. However, with decreasing processing temperature, the efficiency of the TiO2-coated membrane also decreases. Already at 275 1C (ISM/TiO2/275), the efficiency is comparable to that of the ZnO-coated one, processed at much lower temperatures (ISM/ZnO/100). Therefore, for the strongest effects, one has to coat the membrane at a high temperature, thereby somewhat damaging the morphology of the original ISM. Since most biological templates have a tendency to decompose or deform at high temperatures (pyrolysis temperature E240 1C),44 a deposition at such temperatures is not suitable in most cases. A good compromise can be found if the sensitive membranes are coated with ZnO at 100 1C, showing reasonably efficient photocatalytic behavior. Thus, in terms of bactericidal efficiency as well as preservation of the original morphology, the ISM/ZnO is more beneficial than ISM/TiO2. 4.2

Mechanical flexibility and thermal stability

Even though the ESM is stable against the reaction byproducts of the ALD process (e.g. isopropanol),24,25 as stated above, upon heating (around 240 1C) it undergoes pyrolysis.44 For coating of the ISM with ZnO, the pyrolysis is not a critical issue, the highest photocatalytic efficiency and preservation of the original structures of ISM can be assured by virtue of low processing temperatures (o240 1C). In contrast, in the case of TiO2, due to the required higher processing temperature (4240 1C), even though the photocatalytic efficiency can be assured, the mechanical stability was reduced by the pyrolytic damage to the original structures of the ISM. The results from our experiments are shown in Fig. 5 and Table 2. The resulting ISM/TiO2/275 membranes deposited at 275 1C were more brittle and stiffer than the native ISM (decreased maximum strain emax and increased initial Young’s This journal is

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Fig. 5 Tensile test data of the native ISM, ISM/ZnO/100 and ISM/TiO2/275 membrane and a photograph of the ISM/ZnO/100. As shown in the s–e curve, after low temperature (100 1C) ALD of ZnO, the mechanical properties of ISM/ZnO/100 were enhanced and showed high flexibility, as can be seen from the inset photograph. In contrast, in the case of ISM/TiO2/275, it was observed that the membranes become stiffer after high temperature (275 1C) ALD, presumably caused by thermal damage of the collagen structure.

modulus, Eini(ISM/TiO2/275)). In contrast, the ISM/ZnO/100 membrane showed an even higher flexibility and mechanical stability against external load than the native ISM (increased maximum stress smax and strain emax together with increased initial Young’s modulus Eini(ISM/ZnO/100)). Considering that most of the metal oxides are generally brittle even at nanometer thicknesses45, the ISM membranes after ALD are expected to show lower flexibility and stability to external load, if the contribution of the metal oxide layer itself and thermal effects are considered. However, this is not the case. It is known that the collagen based ESM contains functional groups, such as amines, amides and carboxylates24,25 which may interact with the ALD precursors (TIP or DEZ/water) during the deposition. During the alternating exposure/purge sequence of the ALD precursor pairs, the highly reactive precursors chemically interact with the ISM fiber surface as well as the bulk of the protein structures (results will be published elsewhere). Hence the flexibility of those composite membranes can presumably be ascribed to anchored precursors containing metal compounds, such as Zn or Ti, similar to the mechanical properties enhancing effects of insect’s cuticles by small amounts of impregnated metals.46

5. Conclusions In conclusion, eggshell membranes were used as templates for coatings with TiO2 and ZnO, respectively, via ALD. The resulting structures satisfy the optimal combination of original functionality of the biotemplate and appropriate metal oxides which can improve the functionality of the resulting structures. The membranes show good mechanical flexibility for practical use. Depending on the deposition temperature of the metal oxides, the resulting films were either amorphous or polycrystalline. Upon UV illumination, the ISM/TiO2 and Phys. Chem. Chem. Phys., 2009, 11, 3608–3614 | 3613

ISM/ZnO membranes clearly exhibited bactericidal effects. Above all, it was found that polycrystalline ISM/ZnO membranes can be prepared at a fairly low temperature (100 1C) and nevertheless show bactericidal efficiency which is competitive with that of ISM/TiO2 membranes prepared at a much higher temperature (275 1C). Furthermore, the ZnO-coated membranes are mechanically more stable than the TiO2-coated ones. We conclude that for coatings of diverse temperature sensitive templates (such as biological materials or polymers), low-temperature ALD of ZnO is more suitable than the deposition of TiO2, i.e. thermally less destructive and photocatalytically competitive.

Acknowledgements The authors are grateful to Dr Woo Lee, Dr Andriy Lotnyk, Dr Stephan Senz and Prof. Dietrich Hesse for their contributions to the X-ray measurements and helpful discussions. This work has received financial support from the German Federal Ministry of Education and Research (BMBF, FKZ 03X5507).

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