Field effect transistors based on semiconductive microbially synthesized chalcogenide nanofibers

Acta Biomaterialia 13 (2015) 364–373

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Field effect transistors based on semiconductive microbially synthesized chalcogenide nanofibers Ian R. McFarlane a, Julia R. Lazzari-Dean b, Mohamed Y. El-Naggar a,c,⇑ a

Department of Physics and Astronomy, University of Southern California, 920 Bloom Walk, Seaver Science Center 215C, Los Angeles, CA 90089-0484, USA Department of Chemistry, University of Southern California, Los Angeles, CA 90089-0484, USA c Molecular and Computational Biology Section, Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0484, USA b

a r t i c l e

i n f o

Article history: Received 27 June 2014 Received in revised form 3 October 2014 Accepted 4 November 2014 Available online 11 November 2014 Keywords: Shewanella Arsenic sulfide Nanostructures Field effect transistor Biogenic materials

a b s t r a c t Microbial redox activity offers a potentially transformative approach to the low-temperature synthesis of nanostructured inorganic materials. Diverse strains of the dissimilatory metal-reducing bacteria Shewanella are known to produce photoactive filamentous arsenic sulfide nanomaterials by reducing arsenate and thiosulfate in anaerobic culture conditions. Here we report in situ microscopic observations and measure the thermally activated (79 kJ mol 1) precipitation kinetics of high yield (504 mg per liter of culture, 82% of theoretical maximum) extracellular As2S3 nanofibers produced by Shewanella sp. strain ANA-3, and demonstrate their potential in functional devices by constructing field effect transistors (FETs) based on individual nanofibers. The use of strain ANA-3, which possesses both respiratory and detoxification arsenic reductases, resulted in significantly faster nanofiber synthesis than other strains previously tested, mutants of ANA-3 deficient in arsenic reduction, and when compared to abiotic arsenic sulfide precipitation from As(III) and S2 . Detailed characterization by electron microscopy, energy-dispersive X-ray spectroscopy, electron probe microanalysis and Tauc analysis of UV-vis spectrophotometry showed the biogenic precipitate to consist primarily of amorphous As2S3 nanofibers with an indirect optical band gap of 2.37 eV. X-ray diffraction also revealed the presence of crystalline As8S9-x minerals that, until recently, were thought to form only at higher temperatures and under hydrothermal conditions. The nanoscale FETs enabled a detailed characterization of the charge mobility (10 5 cm2 V 1 s 1) and gating behavior of the heterogeneously doped nanofibers. These studies indicate that the biotransformation of metalloids and chalcogens by bacteria enables fast, efficient, sustainable synthesis of technologically relevant chalcogenides for potential electronic and optoelectronic applications. Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. This is an open access article under the CC BY-NCND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

1. Introduction The synthesis of nanomaterials by biological or biomimetic means in physiological conditions offers multiple advantages over traditional physical and chemical strategies that typically require more extreme environments (temperature, pressure and pH). In addition to the promise of cheaper and greener synthesis processes, the resulting biogenic materials can exhibit unique morphologies and physical/chemical properties stemming from the tight control organisms exert over the composition, nucleation, crystallography and desired function of these materials [1]. While significant attention has been dedicated to understanding the synthesis and structure–function relations of the most abundant ⇑ Corresponding author at: Department of Physics and Astronomy, University of Southern California, 920 Bloom Walk, Seaver Science Center 215C, Los Angeles, CA 90089-0484, USA. Tel.: +1 (213) 740 2394; fax: +1 (213) 740 6653. E-mail address: [email protected] (M.Y. El-Naggar).

biominerals, especially carbonates and phosphates, the last decade has also witnessed additional interest in exploiting biological, especially microbial, strategies for producing a wider range of synthetic materials with technologically relevant mechanical, optical, electronic and magnetic functionalities [2–4]. Towards this goal, recent reports [5–7] demonstrated the synthesis of extracellular chalcogenide nanostructures with unique optoelectronic properties using a bacterial process relying on anaerobic respiration and detoxification activities to alter the oxidation states of the metal, metalloid and chalcogen precursors. Chalcogenide compounds, resulting from the reaction of group VI elements (particularly S, Se and Te) with more electropositive elements (e.g. As, Sb, Si, Ge, Zn, Cd), represent an intriguing target for biogenic synthesis. Chalcogenides have been described as ‘‘chameleon’’ compounds because of their remarkable versatility: depending on composition and synthesis techniques they may be crystalline, glassy, metallic, semiconductive or ionic conductors

http://dx.doi.org/10.1016/j.actbio.2014.11.005 1742-7061/Ó 2014 Acta Materialia Inc. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

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[8]. This versatility leads to a wide range of tunable functionalities in various components including sensors, waveguides, photonic crystals [9] and photoactive devices [10–12]. Chalcogenide glasses are already commercially important in write-once and rewritable optical storage disks as well as phase-change memory relying on amorphous–crystalline transformations [8]. Some members of this family (e.g. As2S3) are infrared-transparent (700 nm–11.5 lm) and are therefore candidate materials for applications in infrared devices [9,13]. From an energy conversion standpoint, chalcogenides have been intensively investigated as photovoltaic materials for solar cells [12]. In addition, AsxSy and AsxSey glasses have been reported to exhibit an optomechanical effect [10,11] for direct light-to-mechanical energy conversion when irradiated with polarized light matching the band gap energy. This phenomenon has been exploited to generate mechanical strain, resulting in all-optical (electricity-free) actuation of chalcogenide-coated cantilevers [10]. Further interest in unique and tunable size-dependent properties has motivated the development of quasi-one-dimensional (nanotube and nanowire) chalcogenides. The majority of these efforts, however, focus on physical and chemical synthesis techniques requiring templates, precursors, and hydro- or solvothermal methods, typically under relatively extreme conditions [14]. More recently, Hur et al. reported a microbiological route for synthesizing chalcogenide nanostructures by exploiting dissimilatory metal-reducing bacteria, specifically a number of Shewanella species, to produce an extracellular network of filamentous arsenic sulfide nanofibers/nanotubes in anaerobic culture conditions [5,6]. This process relies on the remarkable metabolic versatility of Shewanella [15,16] to concomitantly reduce S2O23 to S2 and As(V) to As(III). In this system, the thiosulfate S2O23 serves as a terminal electron acceptor for respiration in lieu of O2 under anaerobic conditions, resulting in S2 , while arsenate reduction is thought to occur via As reductases tied to either the respiration or detoxification pathways of Shewanella. Rather surprisingly, it was reported that the resulting amorphous and polycrystalline nanostructures behaved as simultaneously metallic and semiconductive in terms of their electrical and photoconductive properties, respectively [5]. An additional report demonstrated the incorporation of more elements (Cd, Se) into As–S nanostructures through biogenic deposition and/or abiotic cation exchange to create ternary (As–S– Se and As–Cd–S) and quaternary (As–Cd–S–Se) composites [7]. Using X-ray absorption near-edge structure (XANES) and Fourier transformed extended X-ray absorption fine structure (EXAFS) analyses, the previous reports also confirmed the elemental oxidation states within the biogenic material to be consistent with As2S3 [5,7]. In this study, we present in situ microscopic observations to characterize the microbial synthesis of individual arsenic sulfide nanofibers, measure the synthesis kinetics, and detail the structural, crystallographic, electronic and band gap properties of the nanofibers resulting from the reduction activity of Shewanella. In contrast to previous detailed studies of chalcogenide synthesis by Shewanella sp. strain HN-41 [5,7], we focused our attention on Shewanella oneidensis MR-1 as well as Shewanella sp. strain ANA-3 and mutants of strain ANA-3 deficient in arsenic reduction. In addition to being genetically tractable, which will help shed light on the genetic and biomolecular mechanisms underlying nanomaterial synthesis, strain ANA-3 is widely regarded as the prototypical arsenic reducer, as a result of containing both the detoxification (encoded by ars genes) and respiratory (encoded by arr genes) As(V) reduction pathways [17–19]. The ars pathway is well characterized and known to be present in many bacteria [19,20]. Using this pathway, As(V) enters the cytosol by phosphate transporters and is reduced to As(III) by the arsenate reductase ArsC. As(III) is subsequently extruded from the cells by a cytoplasmic membrane efflux pump, ArsB, which may interact

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with an ATPase subunit, ArsA, to drive As(III) efflux using ATP hydrolysis. In contrast, the arr pathway has only been recently described [18,21]. The arrAB operon of strain ANA-3 encodes a large Mo-containing enzyme, ArrA, and an Fe–S protein, ArrB. Both ArrA and ArrB are required for respiratory reduction of As(V) [18,19]. The use of strain ANA-3 resulted in significantly more rapid precipitation of As–S nanofibers than previously reported under similar conditions. Furthermore, we demonstrate novel field-effect transistors (FETs) based on single biogenic nanofibers, and study their charge mobility and switching behavior as a function of backgating to identify the doping type and majority charge carriers in these semiconductors. 2. Materials and methods 2.1. Bacterial growth A list of the bacterial strains and mutants used in this study is provided in Table 1. The inocula were grown aerobically in 20 ml of LB medium from a frozen ( 80 °C) stock up to an optical density at 600 nm (OD600) of 1.5 ± 0.15. These aerobic pre-cultures were inoculated at 0.1% (v/v) into anaerobic serum bottles each containing 80 mL HEPES-buffered (30 mM) medium consisting of: 20 mM sodium DL-lactate, as electron donor; 28 mM ammonium chloride; 1.34 mM potassium chloride; 4.35 mM sodium phosphate monobasic; 20 mM sodium hydroxide; 10 mM thiosulfate, as Na2S2O3
5H2O; and 5 mM arsenate, as Na2HAsO4
7H2O. Vitamins, amino acids and trace mineral stock solutions were used to supplement the medium as described previously [22]. The medium was adjusted to an initial pH of 7.25, and anaerobic conditions were reached by purging with 100% N2 for in excess of 45 min. The anaerobic serum bottles, sealed with butyl stoppers and aluminum seals, were sterilized by autoclaving at 120 °C for 15 min. Arsenate, thiosulfate and vitamins were added after autoclaving. All cultures were grown at 30 °C and agitated at a rate of 150 rpm. 2.2. Preparation of nanomaterials for EDS measurements, Tauc analysis and transistor microfabrication For each preparation, 1 ml of the As–S precipitate was diluted in 14 ml of ultrapure water (Millipore Milli-Q Integral 5 purification system) and pelleted by centrifugation at 3000 RCF for 20 min. The samples were allowed to settle for a further 15 min before removing the supernatant. The samples were then washed eight times to remove salts, without further centrifugation, allowing 15 min between the addition and removal of ultrapure water for the material to settle at each step. For device fabrication, the resulting yellow precipitates were drop deposited on oxidized silicon chips for 5–15 min before removing the liquid by capillary action using a Kimwipe. The chips were then dried under nitrogen gas. 2.3. In situ microscopy of nanofiber synthesis Microscopy observation chambers (500 lm height, 3 cm2 surface area, 150 ll volume) were constructed by using double-sided tape (Scotch 3 M Permanent) to separate a coverslip (VWR No. 1) from the glass region of a glass-bottom Petri dish (WillCo Wells, GWSt-5030). A 1 mm diameter filling port was created by placing a 0.5 cm length of plastic microtubing in a drilled hole on the top of the Petri dish lid and fixing it in place with epoxy (Devon 5 Minute Gel). All components were sterilized in ethanol and allowed to dry before cell injection. An overnight culture of strain ANA-3 was grown in LB medium to OD600 2.0 and inoculated into the anaerobic defined medium described above at 1% (v/v). Subsequent chamber filling and assembly was performed in a nitrogen bag,

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Table 1 Strains and mutants used in this study and time from inoculation until visible formation of As–S precipitate in medium supplemented with 10 mM thiosulfate and 5 mM arsenate. Strain/mutant

Description

Time to visible precipitate (h)

MR-1 ANA-3 ARRA3 ARSB1 ARM1

Wild-type, Shewanella oneidensis [15] Wild-type, Shewanella sp. [17] DarrA mutant derived from ANA-3; does not respire As(V) [18] arsB::Kan(EZ::TN < KAN-2>); arsB mutant derived from ANA-3; deficient in detoxification of As(V) [17] DarrA DarsC mutant derived from ARRA3; does not reduce As(V) under any condition [19]

144 ± 24 19 ± 2.5 75 ± 10 40 ± 5 40 ± 5

and anaerobic conditions were maintained for the duration of the experiment after transfer to the defined medium. Cells were injected slowly into the 150 ll chamber, avoiding bubbles. The Petri dish lid was sealed to the base with epoxy, and dishes were filled with additional inoculated medium through the previously drilled port to minimize the nitrogen headspace. The filling port was subsequently sealed with epoxy and the sample was placed on an inverted Nikon Eclipse Ti microscope with a heated stage for time-lapse transmission or reflection imaging. The microscope was equipped with a drift correction unit (Nikon Perfect Focus System) for maintaining focus at the dish–medium interface during time-lapse imaging. Images were captured at 5 min intervals during fiber formation and a shutter was used to avoid sample illumination except while actively capturing images. Fluorescence microscopy was also used to assess the localization of the biogenic nanofibers relative to cells as indicated by the NanoOrange protein stain (Life Technologies, catalog no. N-6666). 2.4. Growth kinetics To investigate the growth kinetics of the biogenic nanofibers, we systematically investigated the bulk precipitation of As–S as a function of temperature. For each measurement, Shewanella sp. strain ANA-3 cultures were incubated with arsenate and thiosulfate, as described above, at 30 °C for 16.5 h in order to seed the reduction and precipitation reactions. The cultures were then moved to an incubator already warmed to the temperature of interest and the total precipitate was subsequently pelleted, washed and weighed at regular intervals. First, 40 ml of each 80 ml experiment was centrifuged at 5750 RCF for 5 min, followed by standing still in the vertical position for an additional 15 min to allow the sample to settle. The supernatant was removed and the precipitate from the remaining 40 ml volume was then pelleted in the same container. The supernatant was removed again and the walls of the container were washed with a stream of ultrapure water to remove any precipitate from the walls. The container was then filled to 15 ml with ultrapure water and centrifuged a third time. Each sample was then washed six times to remove salts, as described above for Tauc analysis (Section 2.2) and then dried overnight in air on weigh dishes. Pellets were finally weighed on weigh dishes in triplicate. 2.5. Structural, optoelectronic, and electronic (FET) characterization The biogenic nanomaterials were studied by scanning electron microscopy (SEM) using a JEOL JSM 7001F field-emission microscope equipped for energy-dispersive X-ray spectroscopy (EDS) for elemental analysis. Further quantitative analyses (1–2% accuracy) of stoichiometry were performed by electron probe microanalysis (EPMA) with a JEOL JXA-8200 interfaced to multiple wavelength dispersive X-ray spectrometers (WDS) and featuring reference standards of known composition. Each EPMA volume sampled is typically a few cubic microns, corresponding to a weight of a few picograms. The nanomaterials were also observed by transmission electron microscopy (TEM) using a JEOL 2100F in both imaging (bright-field and dark-field) and diffraction modes with a high tension of 200 kV. The microstructure and crystallinity

of the nanomaterial was also characterized by h–2h X-ray diffraction (XRD) scans on a Rigaku Ultima IV diffractometer. The optical band gap was estimated from Tauc plots (i.e. (ahm)n vs. hm where a is the absorption coefficient and hm is the photon energy) after measuring the UV–vis spectrum using a Thermo Scientific NanoDrop 2000c UV–vis spectrophotometer. For fabrication of nanofiber-based FETs, the nanomaterials were deposited on oxidized silicon chips (1 lm SiO2 layer on degenerately doped Si) with photolithographically pre-patterned Au contact pads as described previously [23,24]. Nanofibers were located by SEM in between the pre-patterned contacts, and source/drain Pt electrodes were deposited using a focused ion beam system (JEOL JIB-4500 multibeam SEM/FIB instrument) equipped with a Pt gas injection system (Oxford Instruments OmniGIS) to connect the gold contact pads to the nanofibers. The underlying doped Si substrate was used for backgating the resulting single-nanofiber FETs. Drain-to-source current vs. voltage (Ids Vds) measurements as a function of gating voltage (Vg) were performed on a Signatone S1160 probe station instrumented to an Agilent 4156C semiconductor parameter analyzer. 2.6. Detection of arsenic Aqueous phase As(V) and As(III) concentrations were measured using an integrated ion chromatography (IC) and atomic fluorescence spectrometry (AFS) system. The IC system was a Dionex GP40 gradient pump within a Dionex LC20 chromatography enclosure connected to a Hamilton PRP-X100 10 lm 4.1  250 mm column. The AFS was a PS Analytical PSA 10.055. Solutions used were: mobile phase of 10 mM K2HPO4 and KH2PO4 adjusted to a pH of 6.25, reductant base of 100 mM NaOH and 530 mM NaBH4, and acid solution of 1.5 M HCl. All reagents and phases were prepared in ultrapure water. Calibration samples were prepared from standard anaerobic growth media with both arsenite and arsenate in 0.63, 0.94, 1.56, 2.19, 3.12 and 5 mM concentrations. Calibration and data samples were diluted to 10 4 of the original concentration using identical procedures and injected into the IC/AFS system. Each calibration point was measured twice; each data point four times. The calibration curve was fitted quadratically, constraining zero area to correspond to zero concentration. Analysis involved baseline removal, integration of peak areas and subsequent comparison to the calibration curve. The As(III) signal peaked from roughly 1.75 to 2.75 min and As(V) from 3.25 to 4.5 min. The signal typically returned to baseline between peaks, indicating sufficient fractionation by the column for accurate analysis and quantification. 3. Results 3.1. Synthesis, in situ microscopy, and growth kinetics of As–S nanofibers The production of As–S was visually detected as a bright yellow precipitate in all cultures incubated with As(V) and S2O23 (Fig. 1). Shewanella sp. strain ANA-3 resulted in rapid precipitation (<1 day) compared to S. oneidensis MR-1 (6 days) (Table 1). Remarkably, all

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three ANA-3 mutants produced As–S precipitate, albeit at later times relative to wild-type (1.7–3.1 days, Table 1), despite the disruption of critical components involved in successful As(V) reduction. SEM revealed that the precipitate consisted exclusively of nanofibers, and nanofiber bundles, ranging in diameter from 20 to 600 nm and reaching up to 150 lm in length. While cells were also routinely observed in the SEM preparations (Fig. 2), the nanofibers were located extracellularly. To shed further light on the mechanism of nanofiber formation, we performed in situ microscopy to measure the growth rate and localization of nanofibers relative to Shewanella sp. strain ANA-3 cells (Fig. 3A–B and Fig. S1). Fiber growth at room temperature started 17 h after the inoculation of the in situ observation chamber, with an initial rate of roughly 10 ± 2 nm min 1 (based on six fibers) (Fig. 3C). The growth rate subsequently declined from this initial value, reaching a steady 3.1 ± 0.4 nm min 1 (based on 45 fibers) within 4 h. While active bacterial cultures are needed to initiate the reduction (non-inoculated control medium with As(V) and S2O23 did not result in precipitation or reduction of As/S, consistent with Ref. [5]), we observed that the nucleation of the nanofibers did not originate at cell bodies. Furthermore, the subsequent extension of the nanofibers generally occurred in the extracellular space, and the extension pattern reflected a tip-growth, rather than base-growth, mechanism (Fig. 3B). By weighing the total precipitate after 2 months of incubation at 30 °C using Shewanella sp. strain ANA-3, we found that the total precipitate yield was 82 ± 8% of the theoretical maximum yield (49.2 mg from each 80 ml batch experiment), calculated based on the starting As and S concentrations used in our experiments and the resulting nanofiber stoichiometry (As2S3—see Section 3.2 and Discussion section below). To investigate the nanofiber growth kinetics, we measured the precipitation rate as a function of temperature (Fig. 4). To avoid the adverse effects of higher temperatures on the mesophilic Shewanella, and since fiber formation started between 16.5 and 21.5 h at 30 °C (Table 1 and Fig. 3), the temperature was only elevated after 16.5 h of incubation at 30 °C. Fig. 4A shows that the nanofiber formation continued at these higher temperatures, approaching a maximum yield similar to that seen for 30 °C. The initial precipitation rate (extrapolated from the initial slope of Fig. 4A) followed an Arrhenius dependence Ea

on temperature with the rate given by Ae RT , where A is a preexponential factor, Ea is the activation energy, R is the universal gas constant and T is the growth temperature. From the Arrhenius plot displayed in Fig. 4B, the activation energy is Ea = 78.9 ± 0.8 kJ mol 1. 3.2. Compositional, structural, and optoelectronic characterization EDS confirmed the presence of As and S in the biogenic nanofibers (Fig. 5). After this initial confirmation of arsenic sulfide formation, the stoichiometry was more quantitatively determined by

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Fig. 2. False color scanning electron microscopy of Shewanella sp. strain ANA-3 cells (blue) and arsenic sulfide nanofibers (yellow). The nanofibers ranged in diameter from 20 to 600 nm and reached 150 lm in length.

EPMA to give the As and S at.%, using 14 measurements across four different locations on a dense As–S preparation. The resulting As:S ratio of 38:62 ± 3% was found to be consistent with an As2S3 stoichiometry. Bright-field TEM images (Fig. 6) did not reveal any grain boundaries or diffraction-related contrast. In addition, selected-area diffraction mode imaging primarily revealed a diffuse ring pattern (inset of Fig. 6) consistent with an amorphous structure [13], except for infrequent diffraction peak patterns found while scanning the sample area (see below). The optical band gap of the As2S3 nanofibers was determined by Tauc plots i.e. (ahm)n vs. hm [25,26] (Fig. 7). The best linear fit to the absorption onset was obtained with n = ½, indicating an indirect band gap semiconductor, and extrapolating to the abscissa gave the band gap Eg,indir = 2.37 ± 0.05 eV (error is standard error). A small fraction of the nanofiber morphologies exhibited periodic branching with conserved angles (Fig. S2), and occasional weak diffraction peaks were observed while scanning across various regions of the precipitate and acquiring TEM diffraction patterns from a high-speed CCD camera (Gatan Orius 200D) (data not shown). The latter approach was used in order to limit the exposure time, since the samples were found to be highly sensitive to beam exposure, making it difficult to acquire diffraction data with conventional means. These observations motivated us to examine the crystallinity of the samples with XRD h–2h scans. The overall XRD pattern presented in Fig. 8 is a close match to the XRD patterns of b-As4S4 (As8S8) [27,28] and alacránite (As8S9) [29], as well as the previously reported AsxS9-x series spanning the composition from b-As4S4 to As8S9 [30]. It is difficult to further

Fig. 1. Incubation of Shewanella sp. strain ANA-3 in a medium supplemented with 20 mM lactate, 10 mM thiosulfate and 5 mM arsenate results in macroscopically visible quantities of arsenic sulfide nanofibers. Images are in increasing magnification taken by (A) optical camera and (B, C) scanning electron microscopy.

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Fig. 3. In situ time-lapse microscopy of nanofiber growth in a Shewanella sp. strain ANA-3 culture. Images displayed in (A) 12 h and (B) 6 h increments. Extension from stationary kinks, as seen in (B), reflects a tip-growth, rather than base-growth, mechanism. (C) Growth rate (mean ± SE) of nanofibers at room temperature extracted from similar time-lapse images.

pinpoint the exact phase, since the alacránite structure is an ordered packing of As4S4 and As4S5, with a molecular arrangement and XRD pattern closely resembling those of b-As4S4. It should be noted that the high beam sensitivity of these minerals has been previously reported [27,28], which is consistent with our observations. Longer incubations resulted in a small increase in XRD peak intensities (Fig. 8), suggesting a modest improvement in the crystallinity of this fraction. In addition to the b-As4S4/As8S9 peaks, we observed a small peak develop over time (2h = 16.5°) consistent with realgar (a-As4S4). 3.3. Single arsenic sulfide nanofiber FETs We constructed FETs based on individual arsenic sulfide nanofibers (NF-FETs) in order to characterize the electronic transport, doping characteristics and gating behavior of the biogenic nanofibers. The NF-FET design schematic and a representative SEM image of a fabricated NF-FET device are presented in Fig. 9. The dependence of the drain-to-source current vs. voltage (Ids Vds) on the

gate voltage (Vg) is shown in Fig. 10. Significantly, two different gating behaviors were observed. Out of 34 successfully fabricated NF-FETs, 21 displayed increased conductance with increasingly negative Vg (Fig. 10A,B). This gate dependence is characteristic of p-type doped nanofibers [31]. Eight devices showed the opposite gate dependence (increased conductance at more positive Vg), which is characteristic of n-type semiconductors (Fig. 10C,D) [31]. The remaining five devices exhibited a more complex behavior (e.g. Fig. S3), likely due to those FET channels consisting of bundles containing heterogeneous nanofibers. The resistivity (including contributions from the metal–nanofiber contact resistances) was estimated from the Ids Vds data at zero gate voltage, yielding 1.78 ± 0.83  105 and 8.9 ± 5.4  104 X cm for the p-type and n-type nanofibers, respectively. These resistivity measurements are consistent with previously reported values in As2S3 thin films [32]. In addition, the carrier field-effect mobility (l) was estimated from the transconductance (oIds/oVg) according to l = (oIds/oVg)(CVds/L2) 1, where L is the nanofiber length and C is the gate capacitance [33,34]. By assuming a cylindrical nanofiber

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Fig. 6. Bright-field TEM imaging of the arsenic sulfide nanofibers. Inset shows a representative selected-area diffraction diffuse pattern consistent with amorphous materials.

Fig. 4. The precipitation kinetics of arsenic sulfide nanofibers. (A) Time and temperature dependence of the precipitate yield as a percentage of the theoretical maximum (100% = 0.62 mg ml 1). Anaerobic Shewanella sp. strain ANA-3 cultures were incubated in a medium supplemented with 20 mM lactate, 10 mM thiosulfate and 5 mM arsenate for 16.5 h at 30 °C (to seed the reduction and precipitation reactions) before the temperature was elevated. (B) Arrhenius plot of the initial precipitation rate dependence on temperature, giving an activation energy, Ea, of 78.9 ± 0.8 kJ mol 1.

Fig. 7. Tauc plot ((ahm)n vs. hm) from UV–vis data for arsenic sulfide nanofibers. Best fits were for n = ½, resulting in an indirect band gap Eg,indir = 2.37 ± 0.05 eV—a good match to amorphous As2S3 (n = ½, Eg,indir = 2.36 eV) rather than crystalline As2S3 (n = 2, Eg,dir = 2.6 eV).

Fig. 8. XRD patterns of the arsenic sulfide nanofibers measured after 5, 20 and 96 day incubations, as indicated. Below are reference XRD patterns for b-As4S4 and alacránite (As8S9), from AMCSD database codes 004217 and 0019016, respectively.

Fig. 5. (A) SEM and corresponding (B) EDS of a single nanofiber, confirming the presence of As and S. Image and spectra collected at 6 kV beam energy and 14.7 mm working distance. The lower-energy C and O peaks from the underlying carbon tape substrate (4.5 and 0.25 kCnts, respectively, and confirmed by measuring the carbon tape separately) are not shown, to enhance the clarity of the single fiber’s As and S peaks. Quantitative EPMA subsequently resulted in an As:S ratio of 38:62 ± 3%, consistent with As2S3.

geometry, C  2peeoL/ln(2h/r), where e is the dielectric constant of the SiO2 gate insulator, eo is the permittivity of free space, h is the oxide thickness and r is the nanofiber radius [31]. Using this procedure, the mobility was found to be 4.3 ± 1.6  10 5 and 4.6 ± 2.9  10 5 cm2 V 1 s 1 for the p-type and n-type devices, respectively.

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Fig. 9. Nanofiber field effect transistors (NF-FETs). (A) Device schematic showing source and drain electrodes (labeled S and D) contacting a nanofiber. The underlying degenerately doped Si substrate acts as a gate (labeled G). Also displayed are the thin SiO2 layer (grey) and focused ion beam deposited Pt electrodes (purple) contacting the nanofiber. (B) SEM image of a representative device showing rectangular Pt depositions connecting the nanofiber to the Au source-drain electrodes.

4. Discussion Microbes play a major role in the biotransformation of all redox-active elements in the biosphere, including metals, metalloids and chalcogens [16]. Microbes control these biotic–abiotic interactions to achieve a number of different objectives, ranging from detoxification to energy generation through the use of reduced or oxidized elements as electron donors or acceptors, respectively, for respiration [35]. In addition to the fundamental consequences for global elemental cycles [36], these microbial

redox activities may be harnessed for bioremediation (treatment of pollutants) and biotechnology applications including biosensors, biocatalysis and electricity generation in microbial fuel cells [35,37]. With the increased interest in biomineralization and biogenic materials [1], a number of studies have also demonstrated the control of microbial redox activity to synthesize unique nanomaterials including magnetic Fe3O4 [38], microtubular Fe2O3 oxides as potential Li-ion battery anodes [39,40], goethite nanowires [41], Se/Te nanoparticles [42,43], Ag2S [3], and precious metals such as Au nanoparticles [4,35,44]. Recent reports also demonstrated the controlled synthesis of Ag and Cu nanostructures using silver-resistant Morganella species, and an uptakereduction-efflux mechanism (broadly similar to the ars arsenic resistance pathway available in strain ANA-3) was proposed to explain the biosynthesis process [45,46]. Most relevant to this study, Lee et al. recently demonstrated a pioneering method for the production of novel filamentous As–S nanostructures using a number of Shewanella strains, including strain HN-41, to reduce As(V) and S2O23 under anaerobic conditions [5,6]. These studies inspired us to explore the synthesis of arsenic sulfide nanofibers by another Shewanella strain, the model As(V) reducer strain ANA-3, and to study the applicability of these chalcogenide nanostructures as building blocks in potential nanoscale devices. Our primary objectives were to elucidate the nanofiber growth mechanism, enhance the precipitation kinetics, characterize the structural/optoelectronic properties and to demonstrate functional FETs based on these biogenic nanomaterials. Many Shewanella strains can use thiosulfate as a respiratory electron acceptor, thereby reducing it to sulfide [37]. Successful precipitation of arsenic sulfide also requires the reduction of As(V) to As(III). We hypothesized that the use of strain ANA-3, capable of expressing both the ars and arr genes encoding the detoxification and respiratory As(V) reduction systems [18,19], will result in faster synthesis of As2S3 nanofibers relative to strain HN-41 whose genome contains only the ars detoxification pathway [47]. Indeed, visible precipitate was observed within 19 ± 2.5 h for

Fig. 10. Electrical transport characteristics of the p-type and n-type nanofiber FETs. (A) The dependence of the drain-to-source current vs. voltage (Ids Vds) at different Vg from 20 to +20 V and (B) the corresponding transfer (Ids Vg) curve at |Vds| = 2 V, demonstrating p-type behavior. (C) Ids Vds for Vg from 40 to 40 V and (D) the corresponding transfer (Ids Vg) curve at |Vds| = 2 V, demonstrating n-type behavior.

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ANA-3 cultures incubated with arsenate and thiosulfate; this response is significantly faster than previously observed in other Shewanella strains [6], and our own results with S. oneidensis MR-1 under identical conditions (Table 1). MR-1 does not have an identifiable respiratory As(V) reductase (arrA) and its putative detoxification As(V) reductase (arsC) has <60% sequence similarity with arsC from ANA-3 [6]. No precipitation was observed in non-inoculated control media containing As(V) and S2O23 or As(V) and S2 [5]. These abiotic controls confirm that active microbial cultures are necessary for the precipitation of As2S3 nanofibers from As(V) and S2O23 . With this in mind, we were quite surprised to observe the delayed formation of nanofibers by ANA-3 mutants disrupted in one or both of the detoxification and respiratory As(V) reduction pathways (Table 1). In particular, the ability of the ARM1 (missing both the arsC and arrA As(V) reductases) strain to synthesize As2S3 nanofibers, despite being previously shown ([19] and confirmed here) not to reduce As(V), suggests an additional microbially influenced mechanism of As(V) reduction under our experimental conditions. To investigate this mechanism of delayed nanofiber synthesis by strains disrupted in As(V) reduction, we performed IC/AFS measurements of As ion concentrations in the abiotic control containing As(V) (5 mM) and S2 (10 mM as Na2S), and observed a modest slow reduction of As(V) to As(III) despite the lack of precipitate (Fig. S4, 0.5 mM As(III) observed after 6.5 days). This finding is consistent with previous studies of abiotic As(V) reduction by dissolved S2 , demonstrating slow kinetics at neutral pH [48], although we cannot rule out possible reductive contributions from additional chemicals in the growth medium. The abiotic reduction of arsenate observed here suggests that microbial strains unable to reduce As(V) directly, such as ARM1 [19], can influence partial As(V) reduction indirectly after producing S2 from the respiratory reduction of S2O23 . This indirect mechanism has slower kinetics, however, than direct As(V) reduction by wild-type ANA-3 where the presence of As reductases (ArrA and ArsC) was correlated with significantly faster precipitation rates (Table 1). In both the direct and indirect mechanisms, reduced S2 and As(III) are necessary for the precipitation of the As–S nanofibers. An additional abiotic control containing reduced As and S (As(III) and S2 , as Na2S) did result in the precipitation of nanofibers but at a significantly lower rate and smaller yield compared to incubation of As(V) and S2O23 with strain ANA-3, as measured by As2S3 absorption at 375 nm (Fig. S5). In other words, bacterial synthesis of nanofibers was faster and more effective than the abiotic precipitation of already reduced As and S. These results indicate that, beyond an active role in reduction, Shewanella cells play an additional role in catalyzing the nucleation of nanofibers from reduced As(III) and S2 . We observed a significant reaction yield with strain ANA-3; the As2S3 precipitate reached >80% of the maximum theoretical yield of each incubation after 60 days (Fig. 4). This theoretical yield is estimated by considering that the original 5 mM arsenate can yield a maximum 2.5 mM of As2S3 per liter in excess S conditions, and using the As2S3 molecular weight of 246 g mol 1, resulting in a maximum yield of 49.2 mg for each 80 ml incubation (0.62 mg ml 1). In addition to evaluating the overall precipitation yield, we characterized the nanofiber growth rates and precipitation rates during active synthesis. Our in situ observations (Fig. 3) revealed a decline in the growth rates of individual nanofibers with increased incubation time (from 10 to 3 nm min 1 over 5 h). This observation is consistent with a limitation brought about by the diminishing concentration of reactants in solution, namely As(III) and S2 , as they get incorporated into the nanofibers over time. By measuring the temperature dependence of the precipitation in bulk cultures over time (Fig. 4), we were able to describe the initial precipitation rates with simple thermally

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activated Arrhenius kinetics, and estimated an activation energy of 78.9 ± 0.8 kJ mol 1. Remarkably, this activation energy from our microbially driven process is consistent with metal chalcogenide thin film growth (85 and 68 kJ mol 1 for CdS and CuxS, respectively) by abiotic chemical bath deposition techniques [49,50]. The biological synthesis process, however, avoids the use of toxic solvents and harsh reaction conditions (e.g. temperature and pH) typical of well-established physicochemical strategies [2]. Taken collectively, the EPMA stoichiometry, TEM imaging, diffraction patterns and the indirect (n = ½) 2.37 ± 0.05 eV band gap, in excellent agreement with amorphous As2S3 (n = ½, Eg,indir = 2.36 eV [51]) but not the direct band gap of crystalline As2S3 (n = 2, Eg,dir = 2.6 eV [52]), point to the nanofibers as being primarily amorphous As2S3 (Figs. 5–7). However, we also observed occasional diffraction patterns containing peaks while scanning samples in the TEM, suggesting a crystalline fraction of the precipitate, which was subsequently confirmed by XRD (Fig. 8). This XRD pattern matched the expected patterns of b-As4S4 and As8S9 (alacránite), with both microdomains possibly contained in the previously characterized As8S9-x series [29]. While the presence of these crystalline stoichiometries is clear, they appear to represent only a small fraction of the precipitate, given the overall 38:62 ± 3% As:S stoichiometry measured by EPMA. Until recently, it was thought that b-As4S4 and As8S9 are only produced abiotically at higher temperatures and hydrothermal conditions. Two recent studies, however, demonstrated the formation of these minerals through the action of newly isolated As(V)-reducing bacteria [53,54]. The present study adds a new example of the formation of these minerals by bacteria, specifically Shewanella. The construction of NF-FETs allowed us to both characterize the electronic properties and test the applicability of microbially synthesized nanofibers in a device context. The Ids Vds behavior, especially in the low-bias regime, was roughly linear, suggesting near-ohmic contacts with the electrodes [31]. 62% of the devices tested exhibited the p-type behavior of decreased conductance as Vg becomes more positive. This is explained by the depletion of holes as the p-type semiconductor bands (bent up at the nanofiber–metal interface) are lowered at Vg > 0, thereby suppressing the conductivity [31,34]. The observation of p-type behavior in the majority of devices is again consistent with the behavior of amorphous chalcogenide glasses, including As2S3, that typically exhibit hole conduction; this is in contrast to crystalline As2S3 where electrons are more mobile [55,56]. 24% of the FETs demonstrated the reverse characteristics of increased conductance at Vg > 0; this behavior is explained by the accumulation of electrons in n-type nanofibers as the bands (bent down at the nanofibermetal interface) are lowered [31,34]. The heterogeneity of the nanofibers, in terms of dopant type, may reflect the complexity of the bacterial growth medium containing multiple elements in addition to As and S (see Materials and methods section). While any residual salt and nutrient content appears to be below the detection limit of EDS (0.1 wt.% [57]) as a result of the extensive washing procedure (Section 2.2), it is possible that trace elements may impact the electronic properties. Specifically, the residual elements may be responsible for the observed n-type doping in a fraction of the tested As2S3 nanofibers, which are otherwise known to exhibit p-type conduction intrinsically [55]. These observations also raise the interesting prospect of ‘biological doping’ that may influence, or tune, the properties of the biogenic nanomaterials depending on the constituents of the growth medium. In addition to the p-type and n-type behavior of individual nanofibers, a number of devices exhibited more complex gate dependencies, such as the mixed behavior seen in Fig. S3A,B. This unusual gate dependence was explained by a close inspection of such devices at the electrode–fiber interface (Fig. S3C), revealing that the semiconducting channel consisted of a bundle of

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heterogeneous fibers. While the underlying reason for the bundling of smaller fibers is not yet clear, this phenomenon partially explains the significant diversity of diameters (20–600 nm) observed in our study, since smaller-diameter nanofibers may coalesce into larger-diameter structures. It should be noted that no effort was made to improve the overall device performance by annealing, which may further decrease both the nanofiber and nanofiber–electrode contact resistances, since our primary goal was to assess the as-synthesized nanomaterials. From the transconductance of the NF-FETs, we extracted field-effect hole and field-effect electron mobilities of 4.3 ± 1.6  10 5 and 4.6 ± 2.9  10 5 cm2 V 1 s 1 for the p-type and n-type nanofibers, respectively. The p-type mobility is in excellent agreement with the previously observed hole mobility (10 4–10 5 cm2 V 1 s 1) in amorphous As2S3 glasses [55,56]. The biogenic NF-FET mobility demonstrated here is significantly lower than many well-studied FETs based on crystalline or organic semiconductors [34,58]. While this results in small (pA) on currents and on/off current ratios, it should be noted that the p-type devices showed attractive threshold voltages (Vg  0 V). Future applications may also rely on the 2.37 eV optical band gap of the biogenic As2S3, which compares well to the 2.42 eV band gap of CdS, a technologically important chalcogenide widely used in commercial photoresistors, and actively pursued for applications in photonics, photovoltaics and transistors [59]. For this reason, we are currently investigating the use of biogenic As2S3 as the active component in photoelectrochemical cells. Our results motivate further investigations geared towards improving the electronic and optoelectronic characteristics of cheaply and greenly produced biogenic nanomaterials. 5. Conclusions Biological, including microbial, systems present unique opportunities for the economic and eco-friendly fabrication of nanomaterials with technologically relevant mechanical, optical, electronic and magnetic functionalities. In this study, we harnessed the As and S reductase activity of Shewanella sp. strain ANA-3 to drive the high yield precipitation (504 mg per liter of culture) of extracellular As2S3 nanofibers. The synthesis rates by strain ANA-3, which possesses both the detoxification and respiratory As(V) reduction pathways, were more rapid than previous observations using other Shewanella strains. Direct in situ observations of nanofiber growth, and bulk measurements of the precipitation rates, demonstrated thermally activated kinetics with an activation energy of 79 kJ mol 1. The compositional, structural and optoelectronic properties of the nanofibers were characterized by SEM, EDS, EPMA, TEM, XRD and Tauc analysis of UV–vis spectrophotometry, revealing a primarily amorphous As2S3 structure. In addition, we demonstrated and characterized novel FETs based on individual biogenic nanofibers, and detailed the carrier type, mobility and switching behavior of these devices. Given the remarkable technological versatility of chalcogenides, the rapid and high-yield biofabrication process described here may help realize the potential of these nanomaterials in (opto)electronics, sensors, waveguides, photovoltaics and storage devices. Acknowledgments The authors acknowledge Andrea Cheung for input into the bacterial cultivation, Frank Devlin for training and access to XRD, and Dr. Tom Yuzvinsky for microfabrication of the pre-patterned Si chips. EPMA measurements were performed at the Caltech GPS division analytical facility with the help of Dr. Chi Ma. Wild-type ANA-3 and mutants were kindly provided by Profs. Dianne Newman (Caltech) and Chad Saltikov (UCSC). SEM, TEM and FIB

deposition were performed at the USC Center for Electron Microscopy and Microanalysis, where John Curulli and Dr. Matt Mecklenburg provided valuable assistance. We are also grateful to Guang-Sin Lu and Prof. Jan Amend for help and access to the IC/AFS system. Michael Qian and Brian Zukotynski provided assistance in overnight UV–vis measurements. M.E.-N. acknowledges support from NASA through the NASA Astrobiology Institute under cooperative agreement NNA13AA92A. Appendix A. Figures with essential colour discrimination Certain figures in this article, particularly Figs. 4, 5, 7, 9 and 10 are difficult to interpret in black and white. The full colour images can be found in the on-line version, at http://dx.doi.org/10.1016/ j.actbio.2014.11.005. Appendix B. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.actbio.2014. 11.005. References [1] Estroff LA. Introduction: biomineralization. Chem Rev 2008;108:4329–31. [2] Bansal V, Bharde A, Ramanathan R, Bhargava SK. Inorganic materials using ‘unusual’ microorganisms. Adv Colloid Interfac 2012;179:150–68. [3] Suresh AK, Doktycz MJ, Wang W, Moon JW, Gu BH, Meyer HM, et al. Monodispersed biocompatible silver sulfide nanoparticles: facile extracellular biosynthesis using the gamma-proteobacterium, Shewanella oneidensis. Acta Biomater 2011;7:4253–8. [4] Suresh AK, Pelletier DA, Wang W, Broich ML, Moon JW, Gu BH, et al. Biofabrication of discrete spherical gold nanoparticles using the metalreducing bacterium Shewanella oneidensis. Acta Biomater 2011;7:2148–52. [5] Lee JH, Kim MG, Yoo BY, Myung NV, Maeng JS, Lee T, et al. Biogenic formation of photoactive arsenic-sulfide nanotubes by Shewanella sp strain HN-41. Proc NatL Acad Sci USA 2007;104:20410–5. [6] Jiang S, Lee JH, Kim MG, Myung NV, Fredrickson JK, Sadowsky MJ, et al. Biogenic formation of As-S nanotubes by diverse Shewanella strains. Appl Environ Microbiol 2009;75:6896–9. [7] Jiang S, Liu F, Kim MG, Lim JH, Lee KJ, Choa YH, et al. Synthesis of chalcogenide ternary and quaternary nanotubes through directed compositional alterations of bacterial As-S nanotubes. J Mater Chem 2011;21:10277–9. [8] Greer AL, Mathur N. Materials science—changing face of the chameleon. Nature 2005;437:1246–7. [9] Sundaram SK, Johnson BR, Schweiger MJ, Martinez JE, Riley BJ, Saraf LV, et al. Chalcogenide glasses and structures for quantum sensing. Quantum Sens Nanophoton Devices 2004;5359:234–45. [10] Krecmer P, Moulin AM, Stephenson RJ, Rayment T, Welland ME, Elliott SR. Reversible nanocontraction and dilatation in a solid induced by polarized light. Science 1997;277:1799–802. [11] Stuchlik M, Elliott SR. All-optical actuation of amorphous chalcogenide-coated cantilevers. J Non-Cryst Solids 2007;353:250–62. [12] Scheer R, Schock H-W. Chalcogenide photovoltaics: physics, technologies, and thin film devices. 1st ed. Weinheim: Wiley-VCH; 2011. [13] Johnson BR, Schweiger MJ, Sundaram SK. Chalcogenide nanowires by evaporation-condensation. J Non-Cryst Solids 2005;351:1410–6. [14] Rao CNR, Govindaraj A. Synthesis of inorganic nanotubes. Adv Mater 2009;21:4208–33. [15] Myers CR, Nealson KH. Bacterial manganese reduction and growth with manganese oxide as the sole electron-acceptor. Science 1988;240:1319–21. [16] Nealson KH, Belz A, McKee B. Breathing metals as a way of life: geobiology in action. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 2002;81:215–22. [17] Saltikov CW, Cifuentes A, Venkateswaran K, Newman DK. The ars detoxification system is advantageous but not required for As(V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl Environ Microbiol 2003;69:2800–9. [18] Saltikov CW, Newman DK. Genetic identification of a respiratory arsenate reductase. Proc Natl Acad Sci USA 2003;100:10983–8. [19] Saltikov CW, Wildman RA, Newman DK. Expression dynamics of arsenic respiration and detoxification in Shewanella sp strain ANA-3. J Bacteriol 2005;187:7390–6. [20] Rosen BP. Biochemistry of arsenic detoxification. Febs Lett 2002;529:86–92. [21] Krafft T, Macy JM. Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. Eur J Biochem 1998;255:647–53. [22] Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, et al. Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 2007;73:7003–12.

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