Electroluminescence and Photoluminescence from Nanostructured Diatom Frustules Containing Metabolically Inserted Germanium

Electroluminescence and Photoluminescence from Nanostructured Diatom Frustules Containing Metabolically Inserted Germanium
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  DOI: 10.1002/adma.200800292 Electroluminescence and Photoluminescence fromNanostructured Diatom Frustules ContainingMetabolically Inserted Germanium** By  Clayton Jeffryes, Raj Solanki, Yaswanth Rangineni, Wei Wang, Chih-hung Chang,  and Gregory L. Rorrer* Many living organisms fabricate intricate biogenic silicamaterials that possess unique optical and photonic proper-ties. [1] Recently, cell culture systems have been identified as anexciting new vehicle for biomimetic fabrication of photonicnanostructures. [2] For example, diatoms are a prolific class of single-celled algae which fabricate silica shells called ‘‘frus-tules’’ that possess periodic sub-micrometer-scale features,including two-dimensional pore arrays. Preliminary calcula-tions suggest that the diatom frustule can act as a photoniccrystal to provide resonances in the visible spectral range. [3] Diatom cells fabricate these periodic structures from solublesilicon by a bottom-up, self-assembly process involving silicananoparticle building blocks. [4] This fabrication process can bedirected through bioprocess technology, and towards this end,we recently developed a two-stage photobioreactor cultivationprocess for metabolic insertion of germanium (Ge) to thefrustule biosilica of the diatom  Pinnularia sp . [5] In this Communication, we report that frustule biosilicacontaining metabolically inserted Ge possesses both photo-luminescence (PL) andelectroluminescence (EL)in thevisiblespectral range. In addition, the electroluminescence spectrumpossesses line emissions that are consistent with the calculatedresonance modes in the diatom frustule periodic structure.The diatom frustule consists of an upper and lower valve.Treatment of bioreactor-cultured diatom cells with aqueoushydrogen peroxide removed the organic matter from thefrustule biosilica and separated the valves. A transmissionelectron microscopy (TEM) image of a representative biosilicafrustule valve from the diatom  Pinnularia sp . is presented inFigure 1a. The frustule valve has sub-micrometer featuresconsisting of a linear array of pores, nominally 200nm indiameter, aligned parallel to the transverse axis (Fig. 1b), aswell as nanoscale features lining the base of each pore.Germanium was metabolically inserted into the frustulebiosilica of   Pinnularia sp . by a two-stage cell cultivationtechnique, as described in the Experimental section. We havepreviously shown that this two-stage cultivation techniqueuniformly dispersed Ge within the frustule. [5] After metabolicinsertion of Ge, the overall shape of the frustule valve did notchange. However, the frustule pore array changed. At the endof Stage I of the cultivation, just before addition of soluble Geto the culture medium, the base of each ca. 200nm frustulepore was lined with a thin layer of biosilica containing asubarray of ca. 50nm nanopores (Fig. 1b). However, aftermetabolic insertion of (1.6  0.1) wt% bulk Ge into thefrustulebiosilicaduringStageIIofcultivation,allnewfrustulesgenerated by cell division following Ge addition no longerpossessed the nanopore array lining the base of the frustulepores (Fig. 1c). Once these fine features were removed, thefrustule pore array now strongly resembled a two-dimensionalphotonic crystal slab. The mean pore diameter and the meanpore spacing before and after Ge addition are presented inTable 1.The electroluminescent device structure utilizing the diatomfrustule as the luminescence source is presented in Figure 2. Inorder to fabricate the electroluminescent device, diatomfrustule valves were spin-coated onto an indium tin oxide(ITO) coated glass substrate. Scanning electron microscopy(SEM) images of the spin-coated diatom frustule layer for arepresentative sample confirmed that the diatom valves wereuniformly dispersed on the surface, but the frustules wererandomly oriented in the  x –  y  plane, and some were damaged(Fig. 3). A 400nm thin film of hafnium silicate dielectric wasgrown over the diatom frustule layer by atomic layerdeposition, as previously described. [6] The measured dielectricconstant of vacuum-dried (100 8 C, 1.5h) frustule biosilicabearing 1.6wt % Ge ranged from 4.05 to 3.19 (1.0–1000kHz)versus 3.32 to 2.87 (1.0–1000kHz) for frustule biosilica that didnot contain Ge. However, since the 400 nm hafnium silicatelayer dominated the EL device, its dielectric constant of 4.7 [6] was the major contributor to the electric field.The electroluminescence (EL) spectra emitted by devicesfabricated from diatom frustules that contained 1.6wt % Ge  C  OMM UNI   C AT I   ON [ * ] Dr. G. L. Rorrer, C. Jeffryes, W. Wang, Dr. C.-H. ChangDepartment of Chemical EngineeringOregon State UniversityCorvallis, OR 97330 (USA)E-mail: rorrergl@engr.orst.eduDr. R. Solanki, Y. RangineniDepartment of Electrical and Computer EngineeringPortland State UniversityPortland, OR 97201 (USA)[ ** ] This research was supported by the National Science Foundation(NSF) under Nanoscale Interdisciplinary Research Team (NIRT)award number BES-0400648. Electron microscopy images wereexpertly obtained by Timothy Gutu at the Center for ElectronMicroscopy and Nanofabrication, Portland State University.  Adv. Mater.  2008 ,  20,  2633–2637    2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim  2633      C    O    M    M    U    N    I    C    A    T    I    O    N versus control diatom frustules that contained no Ge arecompared in Figure 4a. Devices fabricated from frustulebiosilicawhichcontainednoGedidnotemitanydetectableELemission at an applied ac voltage of 150V (10kHz), consistentwith previous studies where EL devices fabricated fromthermally grown SiO 2  thin films containing no luminescentcenters did not produce any emission in the 300–700nmrange. [7] In contrast, the EL spectra emitted from diatomfrustules containing 1.6wt % Ge was steady and consisted of aseries of sharp line emissions. Specifically, two bands of ELemission were observed, one in the UV to green range with aseries of line emissions between 300 and 500nm, and the otherin the red to near-IR range with a series of broader emissionsbetween 640 and 780nm. The highest intensity emissionsconsisted of three sharp UV signals at 339nm, 359nm, and382nm. No EL emissions in the green-yellow (500–640nm)range were observed, as the diatom frustule containedno luminescent centers in this range. Control EL devicesfabricated without the diatom frustule layer possessed no ELspectra. Figure 1.  TEM images of the  Pinnularia sp . frustule isolated by hydrogen peroxide treatment of bioreactor-cultured cell mass, focusing on microscalefeatures and the sub-micrometer frustule pore array. a) Representative valve at the end of Stage I of cultivation before metabolic insertion of Ge into thefrustule biosilica. b) Pore array at the end of Stage I of cultivation. c) Pore array of new representative valve at the end of Stage II of cultivation, where thebulk Ge content in the frustule biosilica is now 1.6wt %. The vertical pore alignment lies on the transverse axis (width) of the diatom frustule. Table 1.  Pore dimensions of   Pinnularia sp . frustules before and aftermetabolic insertion of germanium. Frustule Parameter End of Stage ICultivation [0 wt % Ge]End of Stage IICultivation [1.6 wt % Ge]Pore diameter [nm]Transverse 210  12 146  11Axial 197  7 95  11Equivalent diameter 203 124Pore spacing [nm]Transverse 366  9 338  17Axial 313  15 296  7Lattice constant 340  30 317  25Pore area/valve area 0.32 0.12Estimated thickness [nm] 172 133 Figure 2.  Schematic of the EL device structure (not drawn to scale). Figure 3.  SEM images of diatom frustules of   Pinnularia sp . spin-coatedonto the ITO glass surface before atomic layer deposition of the hafniumsilicate dielectric layer. a) Detail of single valve. b) Distribution of valves onsurface. 2634    2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim  Adv. Mater.  2008 ,  20,  2633–2637   C  OMM UNI   C AT I   ON The mechanisms leading to EL emission from ac thin-filmelectroluminescent (ACTFEL) devices are well estab-lished. [8,9] When a large electric field is applied across theelectrodes of an ACTFEL, trapped carriers at the phosphor/insulator interface tunnel out and generate a displacementcurrent within the phosphor. The impact excitation of theluminescent centers in the phosphor by the hot electrons leadsto the optical emission. We propose a similar mechanism forEL from the diatom frustules. The frustule/hafnium silicateinterface is expected to contain traps or interface states. Theapplied ac field will induce tunneling of electrons from thefrustule/silicate interface traps into the frustule, as appliedelectric field is sufficiently large ( > 100MV cm  1 ) to acceleratethese electrons to induce light emission via electron impactexcitation. The EL emission in the UV–green band(300–500nm) can be attributed to the presence of 1.6wt %Ge in silica that leads to formation of defect structures thathave produced EL emission over this spectral range. [10] Theweaker EL emission in the red band ( > 640nm) can beattributed to nonbinding oxygen hole centers, with possiblecontribution from peroxy radicals. [11–14] ThePLspectrumofdiatomfrustulesthatcontained1.6wt%Ge versus control diatom frustules that contained no Ge arecompared in Figure 4b. Both types of diatom frustulespossessed continuous blue photoluminescence with peakemission at 460nm under UV excitation of 337nm. The bluePL most likely srcinates from surface defects on the diatombiosilica, including silanol groups (––Si–OH) and oxygen defectcenters, consistent with previous studies on PL emission frommesoporous silica. [15–18] Biosilica derived from diatom frus-tules are known to possess silanol groups [19] as well asblue–green photoluminescence. [20–22] Amorphous frustulebiosilica that contained metabolically inserted Ge, presumablyin the form of Ge oxides, had a much higher PL intensity.Ge–O defects in amorphous silica are also known to possessblue photoluminescence, [23–26] which would superimpose onthe PL emissions of the diatom biosilica.Ge-implanted SiO 2  thin films commonly possess similar ELand PL spectra. [21] However, since the Ge-doped biosilicafrustules had markedly different EL and PL spectra, it isevident that the PL and EL emission have differentmechanisms. While the srcin of PL is most likely due tointeraction of UV light with defects on the surfaces of themesoporous frustule biosilica, we suggest that the EL resultsfrom higher energy (150V) electronic excitation of the defectcenters within the interior of the Ge-doped biosilica  and  theinteraction of these UV-visible emissions with the periodicholes of the frustule. Optical modes of the diatom frustulemodeled as a photonic crystal slab were calculated usingpore dimensions estimated from TEM images of the frustulevalve (Table 1) and measured refractive index and dielectricconstants. The refractive index of biogenic silica nominallyranges between 1.43–1.48, [1] and so the refractive index of thefrustule biosilica was taken as 1.5 to include the contribution of the 1.6wt % Ge. The frustule pores were filled with hafniumsilicate, with a measured refractive index of 2.26. [6] Normalized optical frequencies versus wave vector for theTEmodeofthediatomperiodicstructureareplottedinFigure5 Figure 4.  Comparison of a) electroluminescence and b) photolumines-cence spectra for diatom frustules that contained no Ge at the end of Stage I of cultivation to diatoms containing 1.6wt % Ge at the end of Stage II of cultivation. Figure 5.  Calculated TE band structure for diatom periodic structureshown in Figure 1c.  Adv. Mater.  2008 ,  20,  2633–2637    2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 2635      C    O    M    M    U    N    I    C    A    T    I    O    N for the average lattice parameters reported in Table 1. Nophotonic band gap in the visible range was predicted from thisphotonic crystal structure. The very bottom line (connec-ting  G – G ) corresponds to the light line, where spontaneousradiationcanbecoupledoutofthephotoniccrystalonlybyleakymodes existing above this light line. Since these frustules werefairly thin ( < 200nm), they could not support a very largenumber of modes. Resonances in the visible spectrum at the Mand X location on the photonic crystal were determined fromFigure 5. For example, M resonances occurred at normalizedfrequencies ( a / l ) of 0.44 and 0.97, which corresponded toresonance wavelengths ( l ) of 745nm and 340nm respectively.Similarly, X resonances occurred at 0.70 (471nm) and 0.95(347nm). These resonance modes were consistent with theobserved line emissions generated by the EL spectra of the devices fabricated with Ge-doped biosilica frustules. Thelowest observed EL emission was 320nm, which was close thepredicted maximum resonance of   a / l ¼ 1 (330nm). To date,resonant emissions corresponding to confined modes in atwo-dimensionalphotonic crystalhaveonlybeenreported fromPL excitation, not EL. [27] With respect to the PL spectra, thepredictedXresonanceat471nmcoincidedwiththeobservedPLmaxima of 460nm.Variations in hole diameter and the lattice constant of two-dimensional photonic crystal slabs can lead to significantchanges in the emission spectrum. [28] Variations in holediameter and lattice constant of the diatom periodic porestructure most likely accounted for the multiple resonancelines recorded from the EL emission. In particular, thevariation in lattice parameter was most likely responsible forproducing the three strong resonance lines in the 340–380nmrange. The brightness of all EL emission lines increasedproportionally with the applied voltage. However, no distinctthreshold voltage was observed, and so these lines were notconsidered as lasing emissions.In summary, we have described the biological fabricationof Ge-doped biosilica frustules by two-stage cell culture of the diatom  Pinnularia , and the incorporation of these diatomfrustules into an electroluminescent device. The electrolumi-nescent properties of these materials were characterized forthe first time, and are uniquely enabled by the metabolicinsertion of Ge into the frustule biosilica and its periodic porestructure. This study represents a first step towards therealization of optoelectronic devices that utilize componentsfabricated through cell culture. More investigation is clearlywarranted to better understand the EL emission mechanismsand to control emission color and brightness. Experimental  Two-Stage Diatom Cell Cultivation : Pure cultures of the photo-synthetic marine diatom  Pinnularia sp . (Ehrenberg) were obtained bythe UTEX Culture Collection of Algae (UTEX# B679). A two-stagephotobioreactor cultivation process developed in our previous work[5] was used to metabolically insert germanium into the silica frustuleof   Pinnularia sp . Bubble-column photobioreactor cultivations werecarried out at 150 m E m 2 s  1 incident light intensity, 14h light/10h darkphotoperiod, 1.0 L air L culture  1 min  1 aeration rate (ca. 350ppmCO 2 ), and 22 8 C. Cultures were grown on LDM/seawater mediumsupplemented with 5.0m M  nitrate and 0.25m M  phosphate. In Stage I of cultivation, diatom cells of initial density of 1.0  10 5  1.6  10 4 cellsmL  1 were grown to silicon starvation on 0.54m M  sodium metasilicate(speciated as Si(OH) 4  at cultivation pH of 8.5) for a total cultivationtime of 140h. Cell division ceased after all the soluble silicon wasconsumed (91h). The cell number yield coefficient was7.69  10 8  1.54  10 8 cells mmol  1 Si, and the final cell density was5.25  10 5  6.50  10 4 cells mL  1 . In Stage II of cultivation, amixture of 1.0mM soluble silicon as Si(OH) 4  and 50 m M germanium asGe(OH) 4  (20 mol Si/mol Ge) was added to the silicon-starved diatomculture, and then the same amount was added again two photoperiods(48h) later. The total silicon added was sufficient to ensure twoadditional cell division cycles, leading to a final cell density of 1.80  10 6  1.14  10 5 cells mL  1 . In the silicon-starved state, bothsilicon and germanium were taken up within 24h after each Si/Geaddition. After 120h cultivation in Stage II, the diatom cells werereplete with silicon and so no more silicon uptake, germanium uptake,or cell division occurred, resulting in final silicon and germaniumcontents in the biomass of 4.0  0.40 mmol Si g  1 dry cell mass and0.116  0.19 mmol Ge g  1 dry cell mass respectively (Si:Ge ratio of 35  6.5 mol Si/mol Ge). Frustule Isolation and Electron Microscopy : Cell biomass wastreated with 30wt % aqueous hydrogen peroxide at pH 2.0 to removeorganic materials and isolate the intact biosilica frustule valves asdescribed previously [5]. Frustule valves were deposited on a holeycarbon copper grid and then imaged by a FEI Tecnai F20 highresolution TEM at 200 keV [5]. Diatom frustules dispersed onITO-coated glass were sputter-coated with gold and then imaged on aFEI Sirion field emission SEM at 1.5 keV. The thickness of the frustulewas estimated from the cell number yield coefficient and TEM imageanalysis of frustule dimensions and porosity by the method adaptedfrom Lewin [29]. STEM-EDS analysis confirmed the frustules werecomposed only of O (0.52keV, K a ) Si (11.74 keV, K a ), and Ge(9.86keVK a 1 ,9.88keVK a 2 ).Thebulkconcentrationofgermaniuminthe frustule biosilica was determined by inductively coupled plasma(ICP) analysis [5]. Electroluminescent Device Fabrication : The EL devices werefabricated on 5  5 cm 2 glass substrates that were precoated with a200nm thick layer of indium tin oxide. Diatom frustule valves isolatedby hydrogen peroxide treatment were dispersed in isopropyl alcoholto concentration of ca. 5  10 6 valves mL  1 and sonicated for 30s. A20 m L aliquot of this suspension was spin-coated (500rpm, 45s) on theITO substrate surface to provide a nominal coverage of 620 valvesmm  2 . These substrates were next loaded into an atomic layerdeposition (ALD) reactor to grow a 400nm thick dielectric film of hafnium silicate as described elsewhere [6]. ALD allowed us toconformally coat the frustules, in particular to fill the frustule poreswith the dielectric. The final processing step consisted of sputterdeposition of 100nm thick, 4 mm diameter aluminum back-electrode.Hence, the device sandwich structure consisted of ITO as the frontelectrode, the frustules coated with hafnium silicate, and Al backelectrode (Fig. 2). Seven duplicate EL devices were fabricated andtested for each sample. Electroluminescence Measurements : For EL measurements, thefront and back electrodes of the device were connected to a powersource that produced a bipolar pulse output, and the EL emission wasrecorded with a CCD detector system. Typical operational frequencywas 10kHz and peak voltage of 150V. The EL emission could beobserved with naked eyes and appeared blue. The brightness increasedwithvoltageandfrequency,andcouldbeoperatedforatleastsixhours.The main limitation was the failure of the Al electrodes, due tooxidationin air. The EL emissionspectraof all seven operating deviceswere almost identical, with slight variations in amplitudes. There wasno EL observed in a set of reference devices made without the diatomfrustules. 2636    2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim  Adv. Mater.  2008 ,  20,  2633–2637   C  OMM UNI   C AT I   ON Photoluminescence Measurements : All PL measurements werecarried out at room temperature. To ensure a uniform sample amountandanalysissurfacearea,2.4mgof frustulepowderwasloadedintothebase of the sample holder, which consisted of square notch (3mm perside and 1.0mm) deep cut into a block of black Delrin polymer. Thelight source was a Spectral Projects ASB-XE-175 EX Xenon lampequipped with a CM100-1/8 monochromator set at 337nm and 0.3mmslit width. The UV beam was aimed at the sample on a 45 8  angle. Theemitted light from the sample was sent through a 420nm UV cut-off filter to remove the reflected excitation signal, focused to a 1.0mmbeam width with a convex lens, and then measured with an ActonInspectrum 300 spectrometer equipped with a CCD detector (0.20mmslit width, 300 gratings mm  1 , 2000ms integration time). Photonic Band Calculations : Photonic band calculations arebased on models provided by Joannopoulos et al., [30] and wereperformed using in-house software similar to the MIT Photonic Bandssoftware. [31] Although the frustule pores were nearly elliptical inshape (Fig. 1), for modeling purposes they were assumed to circularwith equivalent diameterof124nm.The latticesymmetry wasassumedto be square, although in reality it was slightly rectangular. The latticeconstant ( a ) varied from about 320nm to 340nm, and so an averagevalue of 330nm was used for modeling. These parameters were used tocalculate transverse electrical (TE), transverse magnetic (TM), and allother modes for the diatom periodic structure. Dielectric Constant Measurements : The diatom frustule powderwas vacuum dried at 100 8 C for 1.5h. A disk of 6.35mm diameter and0.568mm thickness was prepared by cold uniaxial pressing of diatomfrustule powder at 19.6 bar. Gold thin films were deposited on bothsidesofthepellettoserveaselectrodes.Thedielectricpropertiesofthediatom frustules were measured at 25 8 C by an Agilent 4284A LCRmeter utilizing an environmental chamber at frequencies ranging from1.0 to 1000kHz.Received: January 29, 2008Revised: March 18, 2008Published online: June 2, 2008 [1] J. Aizenberg, V. C. Sundar, A. D. Yablon, J. C. Weaver, G. Chen, Proc. Natl. Acad. Sci. USA  2004  , 101 , 3358. [2] A. R. Parker, H. E. Townley,  Nat. Nanotechnol.  2007  , 2 , 347. [3] T. Fuhrmann, S. Landwehr, M. El Rharbi-Kucki, M. Sumper,  Appl.Phys. B  2004  , 78 , 257. [4] M. Sumper, E. 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