Acta Biomaterialia 13 (2015) 364–373

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Acta Biomaterialia
journal homepage: www.elsevier.com/locate/actabiomat

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
b
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

a r t i c l e i n f o a b s t r a c t

Article history: Microbial redox activity offers a potentially transformative approach to the low-temperature synthesis of
Received 27 June 2014 nanostructured inorganic materials. Diverse strains of the dissimilatory metal-reducing bacteria
Received in revised form 3 October 2014 Shewanella are known to produce photoactive filamentous arsenic sulfide nanomaterials by reducing
Accepted 4 November 2014
arsenate and thiosulfate in anaerobic culture conditions. Here we report in situ microscopic observations
Available online 11 November 2014
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
Keywords:
ANA-3, and demonstrate their potential in functional devices by constructing field effect transistors
Shewanella
Arsenic sulfide
(FETs) based on individual nanofibers. The use of strain ANA-3, which possesses both respiratory and
Nanostructures detoxification arsenic reductases, resulted in significantly faster nanofiber synthesis than other strains
Field effect transistor previously tested, mutants of ANA-3 deficient in arsenic reduction, and when compared to abiotic arsenic
Biogenic materials sulfide precipitation from As(III) and S2 . Detailed characterization by electron microscopy, energy-dis-
persive 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 condi-
tions. 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 biotrans-
formation 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-NC-
ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

1. Introduction biominerals, especially carbonates and phosphates, the last decade

has also witnessed additional interest in exploiting biological,
The synthesis of nanomaterials by biological or biomimetic especially microbial, strategies for producing a wider range of syn-
means in physiological conditions offers multiple advantages over thetic materials with technologically relevant mechanical, optical,
traditional physical and chemical strategies that typically require electronic and magnetic functionalities [2–4]. Towards this goal,
more extreme environments (temperature, pressure and pH). In recent reports [5–7] demonstrated the synthesis of extracellular
addition to the promise of cheaper and greener synthesis pro- chalcogenide nanostructures with unique optoelectronic proper-
cesses, the resulting biogenic materials can exhibit unique mor- ties using a bacterial process relying on anaerobic respiration and
phologies and physical/chemical properties stemming from the detoxification activities to alter the oxidation states of the metal,
tight control organisms exert over the composition, nucleation, metalloid and chalcogen precursors.
crystallography and desired function of these materials [1]. While Chalcogenide compounds, resulting from the reaction of group
significant attention has been dedicated to understanding the syn- VI elements (particularly S, Se and Te) with more electropositive
thesis and structure–function relations of the most abundant elements (e.g. As, Sb, Si, Ge, Zn, Cd), represent an intriguing target
for biogenic synthesis. Chalcogenides have been described as ‘‘cha-
⇑ Corresponding author at: Department of Physics and Astronomy, University of meleon’’ compounds because of their remarkable versatility:
Southern California, 920 Bloom Walk, Seaver Science Center 215C, Los Angeles, CA depending on composition and synthesis techniques they may be
90089-0484, USA. Tel.: +1 (213) 740 2394; fax: +1 (213) 740 6653. crystalline, glassy, metallic, semiconductive or ionic conductors
E-mail address: mnaggar@usc.edu (M.Y. El-Naggar).

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/).
 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373 365

[8]. This versatility leads to a wide range of tunable functionalities with an ATPase subunit, ArsA, to drive As(III) efflux using ATP
in various components including sensors, waveguides, photonic hydrolysis. In contrast, the arr pathway has only been recently
crystals [9] and photoactive devices [10–12]. Chalcogenide glasses described [18,21]. The arrAB operon of strain ANA-3 encodes a
are already commercially important in write-once and rewritable large Mo-containing enzyme, ArrA, and an Fe–S protein, ArrB.
optical storage disks as well as phase-change memory relying on Both ArrA and ArrB are required for respiratory reduction of
amorphous–crystalline transformations [8]. Some members of this As(V) [18,19]. The use of strain ANA-3 resulted in significantly
family (e.g. As2S3) are infrared-transparent (700 nm–11.5 lm) and more rapid precipitation of As–S nanofibers than previously
are therefore candidate materials for applications in infrared reported under similar conditions. Furthermore, we demonstrate
devices [9,13]. From an energy conversion standpoint, chalcoge- novel field-effect transistors (FETs) based on single biogenic
nides have been intensively investigated as photovoltaic materials nanofibers, and study their charge mobility and switching behav-
for solar cells [12]. In addition, AsxSy and AsxSey glasses have been ior as a function of backgating to identify the doping type and
reported to exhibit an optomechanical effect [10,11] for direct majority charge carriers in these semiconductors.
light-to-mechanical energy conversion when irradiated with polar-
ized light matching the band gap energy. This phenomenon has
2. Materials and methods
been exploited to generate mechanical strain, resulting in all-opti-
cal (electricity-free) actuation of chalcogenide-coated cantilevers
2.1. Bacterial growth
[10]. Further interest in unique and tunable size-dependent prop-
erties has motivated the development of quasi-one-dimensional
A list of the bacterial strains and mutants used in this study is
(nanotube and nanowire) chalcogenides. The majority of these
provided in Table 1. The inocula were grown aerobically in 20 ml
efforts, however, focus on physical and chemical synthesis tech-
of LB medium from a frozen ( 80 °C) stock up to an optical density
niques requiring templates, precursors, and hydro- or solvothermal
at 600 nm (OD600) of 1.5 ± 0.15. These aerobic pre-cultures were
methods, typically under relatively extreme conditions [14].
inoculated at 0.1% (v/v) into anaerobic serum bottles each contain-
More recently, Hur et al. reported a microbiological route for
ing 80 mL HEPES-buffered (30 mM) medium consisting of: 20 mM
synthesizing chalcogenide nanostructures by exploiting dissimila-
sodium DL-lactate, as electron donor; 28 mM ammonium chloride;
tory metal-reducing bacteria, specifically a number of Shewanella
1.34 mM potassium chloride; 4.35 mM sodium phosphate
species, to produce an extracellular network of filamentous arsenic
monobasic; 20 mM sodium hydroxide; 10 mM thiosulfate, as
sulfide nanofibers/nanotubes in anaerobic culture conditions [5,6].
Na2S2O3
5H2O; and 5 mM arsenate, as Na2HAsO4
7H2O. Vitamins,
This process relies on the remarkable metabolic versatility of
amino acids and trace mineral stock solutions were used to
Shewanella [15,16] to concomitantly reduce S2O23 to S2 and
supplement the medium as described previously [22]. The medium
As(V) to As(III). In this system, the thiosulfate S2O23 serves as a ter-
was adjusted to an initial pH of 7.25, and anaerobic conditions were
minal electron acceptor for respiration in lieu of O2 under anaero-
reached by purging with 100% N2 for in excess of 45 min. The
bic conditions, resulting in S2 , while arsenate reduction is thought
anaerobic serum bottles, sealed with butyl stoppers and aluminum
to occur via As reductases tied to either the respiration or detoxi-
seals, were sterilized by autoclaving at 120 °C for 15 min. Arsenate,
fication pathways of Shewanella. Rather surprisingly, it was
thiosulfate and vitamins were added after autoclaving. All cultures
reported that the resulting amorphous and polycrystalline nano-
were grown at 30 °C and agitated at a rate of 150 rpm.
structures behaved as simultaneously metallic and semiconductive
in terms of their electrical and photoconductive properties, respec-
tively [5]. An additional report demonstrated the incorporation of 2.2. Preparation of nanomaterials for EDS measurements, Tauc
more elements (Cd, Se) into As–S nanostructures through biogenic analysis and transistor microfabrication
deposition and/or abiotic cation exchange to create ternary (As–S–
Se and As–Cd–S) and quaternary (As–Cd–S–Se) composites [7]. For each preparation, 1 ml of the As–S precipitate was diluted in
Using X-ray absorption near-edge structure (XANES) and Fourier 14 ml of ultrapure water (Millipore Milli-Q Integral 5 purification
transformed extended X-ray absorption fine structure (EXAFS) system) and pelleted by centrifugation at 3000 RCF for 20 min.
analyses, the previous reports also confirmed the elemental oxida- The samples were allowed to settle for a further 15 min before
tion states within the biogenic material to be consistent with As2S3 removing the supernatant. The samples were then washed eight
[5,7]. times to remove salts, without further centrifugation, allowing
In this study, we present in situ microscopic observations to 15 min between the addition and removal of ultrapure water for
characterize the microbial synthesis of individual arsenic sulfide the material to settle at each step. For device fabrication, the result-
nanofibers, measure the synthesis kinetics, and detail the struc- ing yellow precipitates were drop deposited on oxidized silicon
tural, crystallographic, electronic and band gap properties of the chips for 5–15 min before removing the liquid by capillary action
nanofibers resulting from the reduction activity of Shewanella. using a Kimwipe. The chips were then dried under nitrogen gas.
In contrast to previous detailed studies of chalcogenide synthesis
by Shewanella sp. strain HN-41 [5,7], we focused our attention on 2.3. In situ microscopy of nanofiber synthesis
Shewanella oneidensis MR-1 as well as Shewanella sp. strain ANA-3
and mutants of strain ANA-3 deficient in arsenic reduction. In Microscopy observation chambers (500 lm height, 3 cm2 sur-
addition to being genetically tractable, which will help shed light face area, 150 ll volume) were constructed by using double-sided
on the genetic and biomolecular mechanisms underlying nano- tape (Scotch 3 M Permanent) to separate a coverslip (VWR No. 1)
material synthesis, strain ANA-3 is widely regarded as the proto- from the glass region of a glass-bottom Petri dish (WillCo Wells,
typical arsenic reducer, as a result of containing both the GWSt-5030). A 1 mm diameter filling port was created by placing
detoxification (encoded by ars genes) and respiratory (encoded a 0.5 cm length of plastic microtubing in a drilled hole on the top
by arr genes) As(V) reduction pathways [17–19]. The ars pathway of the Petri dish lid and fixing it in place with epoxy (Devon 5 Min-
is well characterized and known to be present in many bacteria ute Gel). All components were sterilized in ethanol and allowed to
[19,20]. Using this pathway, As(V) enters the cytosol by phos- dry before cell injection. An overnight culture of strain ANA-3 was
phate transporters and is reduced to As(III) by the arsenate reduc- grown in LB medium to OD600 2.0 and inoculated into the anaero-
tase ArsC. As(III) is subsequently extruded from the cells by a bic defined medium described above at 1% (v/v). Subsequent
cytoplasmic membrane efflux pump, ArsB, which may interact chamber filling and assembly was performed in a nitrogen bag,
366 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373

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 Wild-type, Shewanella oneidensis [15] 144 ± 24
ANA-3 Wild-type, Shewanella sp. [17] 19 ± 2.5
ARRA3 DarrA mutant derived from ANA-3; does not respire As(V) [18] 75 ± 10
ARSB1 arsB::Kan(EZ::TN < KAN-2>); arsB mutant derived from ANA-3; deficient in detoxification of As(V) [17] 40 ± 5
ARM1 DarrA DarsC mutant derived from ARRA3; does not reduce As(V) under any condition [19] 40 ± 5

and anaerobic conditions were maintained for the duration of the of the nanomaterial was also characterized by h–2h X-ray diffrac-
experiment after transfer to the defined medium. Cells were tion (XRD) scans on a Rigaku Ultima IV diffractometer.
injected slowly into the 150 ll chamber, avoiding bubbles. The The optical band gap was estimated from Tauc plots (i.e. (ahm)n
Petri dish lid was sealed to the base with epoxy, and dishes were vs. hm where a is the absorption coefficient and hm is the photon
filled with additional inoculated medium through the previously energy) after measuring the UV–vis spectrum using a Thermo Sci-
drilled port to minimize the nitrogen headspace. The filling port entific NanoDrop 2000c UV–vis spectrophotometer.
was subsequently sealed with epoxy and the sample was placed For fabrication of nanofiber-based FETs, the nanomaterials were
on an inverted Nikon Eclipse Ti microscope with a heated stage deposited on oxidized silicon chips (1 lm SiO2 layer on degener-
for time-lapse transmission or reflection imaging. The microscope ately doped Si) with photolithographically pre-patterned Au con-
was equipped with a drift correction unit (Nikon Perfect Focus tact pads as described previously [23,24]. Nanofibers were
System) for maintaining focus at the dish–medium interface during located by SEM in between the pre-patterned contacts, and
time-lapse imaging. Images were captured at 5 min intervals source/drain Pt electrodes were deposited using a focused ion
during fiber formation and a shutter was used to avoid sample beam system (JEOL JIB-4500 multibeam SEM/FIB instrument)
illumination except while actively capturing images. Fluorescence equipped with a Pt gas injection system (Oxford Instruments
microscopy was also used to assess the localization of the biogenic OmniGIS) to connect the gold contact pads to the nanofibers.
nanofibers relative to cells as indicated by the NanoOrange protein The underlying doped Si substrate was used for backgating the
stain (Life Technologies, catalog no. N-6666). resulting single-nanofiber FETs. Drain-to-source current vs. voltage
(Ids Vds) measurements as a function of gating voltage (Vg) were
2.4. Growth kinetics performed on a Signatone S1160 probe station instrumented to
an Agilent 4156C semiconductor parameter analyzer.
To investigate the growth kinetics of the biogenic nanofibers,
we systematically investigated the bulk precipitation of As–S as a
2.6. Detection of arsenic
function of temperature. For each measurement, Shewanella sp.
strain ANA-3 cultures were incubated with arsenate and thiosul-
Aqueous phase As(V) and As(III) concentrations were measured
fate, as described above, at 30 °C for 16.5 h in order to seed the
using an integrated ion chromatography (IC) and atomic fluores-
reduction and precipitation reactions. The cultures were then
cence spectrometry (AFS) system. The IC system was a Dionex
moved to an incubator already warmed to the temperature of
GP40 gradient pump within a Dionex LC20 chromatography enclo-
interest and the total precipitate was subsequently pelleted,
sure connected to a Hamilton PRP-X100 10 lm 4.1  250 mm col-
washed and weighed at regular intervals. First, 40 ml of each
umn. The AFS was a PS Analytical PSA 10.055. Solutions used were:
80 ml experiment was centrifuged at 5750 RCF for 5 min, followed
mobile phase of 10 mM K2HPO4 and KH2PO4 adjusted to a pH of
by standing still in the vertical position for an additional 15 min to
6.25, reductant base of 100 mM NaOH and 530 mM NaBH4, and
allow the sample to settle. The supernatant was removed and the
acid solution of 1.5 M HCl. All reagents and phases were prepared
precipitate from the remaining 40 ml volume was then pelleted
in ultrapure water. Calibration samples were prepared from stan-
in the same container. The supernatant was removed again and
dard anaerobic growth media with both arsenite and arsenate in
the walls of the container were washed with a stream of ultrapure
0.63, 0.94, 1.56, 2.19, 3.12 and 5 mM concentrations. Calibration
water to remove any precipitate from the walls. The container was
and data samples were diluted to 10 4 of the original concentra-
then filled to 15 ml with ultrapure water and centrifuged a third
tion using identical procedures and injected into the IC/AFS sys-
time. Each sample was then washed six times to remove salts, as
tem. Each calibration point was measured twice; each data point
described above for Tauc analysis (Section 2.2) and then dried
four times. The calibration curve was fitted quadratically, con-
overnight in air on weigh dishes. Pellets were finally weighed on
straining zero area to correspond to zero concentration. Analysis
weigh dishes in triplicate.
involved baseline removal, integration of peak areas and subse-
quent comparison to the calibration curve. The As(III) signal
2.5. Structural, optoelectronic, and electronic (FET) characterization 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,
The biogenic nanomaterials were studied by scanning electron indicating sufficient fractionation by the column for accurate anal-
microscopy (SEM) using a JEOL JSM 7001F field-emission micro- ysis and quantification.
scope equipped for energy-dispersive X-ray spectroscopy (EDS)
for elemental analysis. Further quantitative analyses (1–2% accu-
racy) of stoichiometry were performed by electron probe micro- 3. Results
analysis (EPMA) with a JEOL JXA-8200 interfaced to multiple
wavelength dispersive X-ray spectrometers (WDS) and featuring 3.1. Synthesis, in situ microscopy, and growth kinetics of As–S
reference standards of known composition. Each EPMA volume nanofibers
sampled is typically a few cubic microns, corresponding to a
weight of a few picograms. The nanomaterials were also observed The production of As–S was visually detected as a bright yellow
by transmission electron microscopy (TEM) using a JEOL 2100F in precipitate in all cultures incubated with As(V) and S2O23 (Fig. 1).
both imaging (bright-field and dark-field) and diffraction modes Shewanella sp. strain ANA-3 resulted in rapid precipitation (<1 day)
with a high tension of 200 kV. The microstructure and crystallinity compared to S. oneidensis MR-1 (6 days) (Table 1). Remarkably, all
 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373 367

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 dis-
ruption of critical components involved in successful As(V) reduc-
tion. 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 nanof-
ibers 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 cham-
ber, 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 ini-
tiate the reduction (non-inoculated control medium with As(V)
and S2O23 did not result in precipitation or reduction of As/S, con- 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
sistent with Ref. [5]), we observed that the nucleation of the nanof-
from 20 to 600 nm and reached 150 lm in length.
ibers 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
EPMA to give the As and S at.%, using 14 measurements across four
base-growth, mechanism (Fig. 3B).
different locations on a dense As–S preparation. The resulting As:S
By weighing the total precipitate after 2 months of incubation
ratio of 38:62 ± 3% was found to be consistent with an As2S3
at 30 °C using Shewanella sp. strain ANA-3, we found that the total
stoichiometry.
precipitate yield was 82 ± 8% of the theoretical maximum yield
Bright-field TEM images (Fig. 6) did not reveal any grain bound-
(49.2 mg from each 80 ml batch experiment), calculated based on
aries or diffraction-related contrast. In addition, selected-area dif-
the starting As and S concentrations used in our experiments and
fraction mode imaging primarily revealed a diffuse ring pattern
the resulting nanofiber stoichiometry (As2S3—see Section 3.2 and
(inset of Fig. 6) consistent with an amorphous structure [13],
Discussion section below). To investigate the nanofiber growth
except for infrequent diffraction peak patterns found while scan-
kinetics, we measured the precipitation rate as a function of tem-
ning the sample area (see below).
perature (Fig. 4). To avoid the adverse effects of higher tempera-
The optical band gap of the As2S3 nanofibers was determined by
tures on the mesophilic Shewanella, and since fiber formation
Tauc plots i.e. (ahm)n vs. hm [25,26] (Fig. 7). The best linear fit to the
started between 16.5 and 21.5 h at 30 °C (Table 1 and Fig. 3), the
absorption onset was obtained with n = ½, indicating an indirect
temperature was only elevated after 16.5 h of incubation at
band gap semiconductor, and extrapolating to the abscissa gave
30 °C. Fig. 4A shows that the nanofiber formation continued at
the band gap Eg,indir = 2.37 ± 0.05 eV (error is standard error).
these higher temperatures, approaching a maximum yield similar
A small fraction of the nanofiber morphologies exhibited peri-
to that seen for 30 °C. The initial precipitation rate (extrapolated
odic branching with conserved angles (Fig. S2), and occasional
from the initial slope of Fig. 4A) followed an Arrhenius dependence
Ea
weak diffraction peaks were observed while scanning across vari-
on temperature with the rate given by Ae RT , where A is a pre- ous regions of the precipitate and acquiring TEM diffraction pat-
exponential factor, Ea is the activation energy, R is the universal terns from a high-speed CCD camera (Gatan Orius 200D) (data
gas constant and T is the growth temperature. From the Arrhenius not shown). The latter approach was used in order to limit the
plot displayed in Fig. 4B, the activation energy is exposure time, since the samples were found to be highly sensitive
Ea = 78.9 ± 0.8 kJ mol 1. to beam exposure, making it difficult to acquire diffraction data
with conventional means. These observations motivated us to
3.2. Compositional, structural, and optoelectronic characterization examine the crystallinity of the samples with XRD h–2h scans.
The overall XRD pattern presented in Fig. 8 is a close match to
EDS confirmed the presence of As and S in the biogenic nanofi- the XRD patterns of b-As4S4 (As8S8) [27,28] and alacránite (As8S9)
bers (Fig. 5). After this initial confirmation of arsenic sulfide forma- [29], as well as the previously reported AsxS9-x series spanning
tion, the stoichiometry was more quantitatively determined by 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.
368 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373

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 gate voltage (Vg) is shown in Fig. 10. Significantly, two different
ordered packing of As4S4 and As4S5, with a molecular arrangement gating behaviors were observed. Out of 34 successfully fabricated
and XRD pattern closely resembling those of b-As4S4. It should be NF-FETs, 21 displayed increased conductance with increasingly
noted that the high beam sensitivity of these minerals has been negative Vg (Fig. 10A,B). This gate dependence is characteristic of
previously reported [27,28], which is consistent with our observa- p-type doped nanofibers [31]. Eight devices showed the opposite
tions. Longer incubations resulted in a small increase in XRD peak gate dependence (increased conductance at more positive Vg),
intensities (Fig. 8), suggesting a modest improvement in the crys- which is characteristic of n-type semiconductors (Fig. 10C,D)
tallinity of this fraction. In addition to the b-As4S4/As8S9 peaks, [31]. The remaining five devices exhibited a more complex behav-
we observed a small peak develop over time (2h = 16.5°) consistent ior (e.g. Fig. S3), likely due to those FET channels consisting of bun-
with realgar (a-As4S4). dles containing heterogeneous nanofibers.
The resistivity (including contributions from the metal–nanofi-
3.3. Single arsenic sulfide nanofiber FETs ber 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
We constructed FETs based on individual arsenic sulfide nanof- the p-type and n-type nanofibers, respectively. These resistivity
ibers (NF-FETs) in order to characterize the electronic transport, measurements are consistent with previously reported values in
doping characteristics and gating behavior of the biogenic nanofi- As2S3 thin films [32]. In addition, the carrier field-effect mobility
bers. The NF-FET design schematic and a representative SEM image (l) was estimated from the transconductance (oIds/oVg) according
of a fabricated NF-FET device are presented in Fig. 9. The depen- to l = (oIds/oVg)(CVds/L2) 1, where L is the nanofiber length and C is
dence of the drain-to-source current vs. voltage (Ids Vds) on the the gate capacitance [33,34]. By assuming a cylindrical nanofiber
 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373 369

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 geometry, C  2peeoL/ln(2h/r), where e is the dielectric constant of
presence of As and S. Image and spectra collected at 6 kV beam energy and 14.7 mm the SiO2 gate insulator, eo is the permittivity of free space, h is the
working distance. The lower-energy C and O peaks from the underlying carbon tape oxide thickness and r is the nanofiber radius [31]. Using this
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
procedure, the mobility was found to be 4.3 ± 1.6  10 5 and
peaks. Quantitative EPMA subsequently resulted in an As:S ratio of 38:62 ± 3%, 4.6 ± 2.9  10 5 cm2 V 1 s 1 for the p-type and n-type devices,
consistent with As2S3. respectively.
370 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373

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 bio-
genic 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 nano-
wires [41], Se/Te nanoparticles [42,43], Ag2S [3], and precious met-
als such as Au nanoparticles [4,35,44]. Recent reports also
demonstrated the controlled synthesis of Ag and Cu nanostruc-
tures using silver-resistant Morganella species, and an uptake-
reduction-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
Fig. 9. Nanofiber field effect transistors (NF-FETs). (A) Device schematic showing
As(V) and S2O23 under anaerobic conditions [5,6]. These studies
source and drain electrodes (labeled S and D) contacting a nanofiber. The inspired us to explore the synthesis of arsenic sulfide nanofibers
underlying degenerately doped Si substrate acts as a gate (labeled G). Also by another Shewanella strain, the model As(V) reducer strain
displayed are the thin SiO2 layer (grey) and focused ion beam deposited Pt ANA-3, and to study the applicability of these chalcogenide nano-
electrodes (purple) contacting the nanofiber. (B) SEM image of a representative
structures as building blocks in potential nanoscale devices. Our
device showing rectangular Pt depositions connecting the nanofiber to the Au
source-drain electrodes. primary objectives were to elucidate the nanofiber growth mecha-
nism, enhance the precipitation kinetics, characterize the struc-
tural/optoelectronic properties and to demonstrate functional
4. Discussion FETs based on these biogenic nanomaterials.
Many Shewanella strains can use thiosulfate as a respiratory
Microbes play a major role in the biotransformation of all electron acceptor, thereby reducing it to sulfide [37]. Successful
redox-active elements in the biosphere, including metals, metal- precipitation of arsenic sulfide also requires the reduction of
loids and chalcogens [16]. Microbes control these biotic–abiotic As(V) to As(III). We hypothesized that the use of strain ANA-3,
interactions to achieve a number of different objectives, ranging capable of expressing both the ars and arr genes encoding the
from detoxification to energy generation through the use of detoxification and respiratory As(V) reduction systems [18,19],
reduced or oxidized elements as electron donors or acceptors, will result in faster synthesis of As2S3 nanofibers relative to strain
respectively, for respiration [35]. In addition to the fundamental HN-41 whose genome contains only the ars detoxification pathway
consequences for global elemental cycles [36], these microbial [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.
 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373 371

ANA-3 cultures incubated with arsenate and thiosulfate; this activated Arrhenius kinetics, and estimated an activation energy
response is significantly faster than previously observed in other of 78.9 ± 0.8 kJ mol 1. Remarkably, this activation energy from our
Shewanella strains [6], and our own results with S. oneidensis microbially driven process is consistent with metal chalcogenide
MR-1 under identical conditions (Table 1). MR-1 does not have thin film growth (85 and 68 kJ mol 1 for CdS and CuxS, respec-
an identifiable respiratory As(V) reductase (arrA) and its putative tively) by abiotic chemical bath deposition techniques [49,50].
detoxification As(V) reductase (arsC) has <60% sequence similarity The biological synthesis process, however, avoids the use of toxic
with arsC from ANA-3 [6]. solvents and harsh reaction conditions (e.g. temperature and pH)
No precipitation was observed in non-inoculated control media typical of well-established physicochemical strategies [2].
containing As(V) and S2O23 or As(V) and S2 [5]. These abiotic con- Taken collectively, the EPMA stoichiometry, TEM imaging,
trols confirm that active microbial cultures are necessary for the diffraction patterns and the indirect (n = ½) 2.37 ± 0.05 eV band
precipitation of As2S3 nanofibers from As(V) and S2O23 . With this gap, in excellent agreement with amorphous As2S3 (n = ½, Eg,indir =
in mind, we were quite surprised to observe the delayed formation 2.36 eV [51]) but not the direct band gap of crystalline As2S3 (n = 2,
of nanofibers by ANA-3 mutants disrupted in one or both of the Eg,dir = 2.6 eV [52]), point to the nanofibers as being primarily
detoxification and respiratory As(V) reduction pathways (Table 1). amorphous As2S3 (Figs. 5–7). However, we also observed occa-
In particular, the ability of the ARM1 (missing both the arsC and sional diffraction patterns containing peaks while scanning
arrA As(V) reductases) strain to synthesize As2S3 nanofibers, samples in the TEM, suggesting a crystalline fraction of the
despite being previously shown ([19] and confirmed here) not to precipitate, which was subsequently confirmed by XRD (Fig. 8).
reduce As(V), suggests an additional microbially influenced mech- This XRD pattern matched the expected patterns of b-As4S4 and
anism of As(V) reduction under our experimental conditions. To As8S9 (alacránite), with both microdomains possibly contained in
investigate this mechanism of delayed nanofiber synthesis by the previously characterized As8S9-x series [29]. While the presence
strains disrupted in As(V) reduction, we performed IC/AFS of these crystalline stoichiometries is clear, they appear to repre-
measurements of As ion concentrations in the abiotic control sent only a small fraction of the precipitate, given the overall
containing As(V) (5 mM) and S2 (10 mM as Na2S), and observed 38:62 ± 3% As:S stoichiometry measured by EPMA. Until recently,
a modest slow reduction of As(V) to As(III) despite the lack of it was thought that b-As4S4 and As8S9 are only produced abiotically
precipitate (Fig. S4, 0.5 mM As(III) observed after 6.5 days). This at higher temperatures and hydrothermal conditions. Two recent
finding is consistent with previous studies of abiotic As(V) reduc- studies, however, demonstrated the formation of these minerals
tion by dissolved S2 , demonstrating slow kinetics at neutral pH through the action of newly isolated As(V)-reducing bacteria
[48], although we cannot rule out possible reductive contributions [53,54]. The present study adds a new example of the formation
from additional chemicals in the growth medium. The abiotic of these minerals by bacteria, specifically Shewanella.
reduction of arsenate observed here suggests that microbial strains The construction of NF-FETs allowed us to both characterize the
unable to reduce As(V) directly, such as ARM1 [19], can influence electronic properties and test the applicability of microbially syn-
partial As(V) reduction indirectly after producing S2 from the thesized nanofibers in a device context. The Ids Vds behavior,
respiratory reduction of S2O23 . This indirect mechanism has slower especially in the low-bias regime, was roughly linear, suggesting
kinetics, however, than direct As(V) reduction by wild-type ANA-3 near-ohmic contacts with the electrodes [31]. 62% of the devices
where the presence of As reductases (ArrA and ArsC) was corre- tested exhibited the p-type behavior of decreased conductance as
lated with significantly faster precipitation rates (Table 1). Vg becomes more positive. This is explained by the depletion of
In both the direct and indirect mechanisms, reduced S2 and holes as the p-type semiconductor bands (bent up at the nanofi-
As(III) are necessary for the precipitation of the As–S nanofibers. ber–metal interface) are lowered at Vg > 0, thereby suppressing
An additional abiotic control containing reduced As and S (As(III) the conductivity [31,34]. The observation of p-type behavior in
and S2 , as Na2S) did result in the precipitation of nanofibers but the majority of devices is again consistent with the behavior of
at a significantly lower rate and smaller yield compared to incuba- amorphous chalcogenide glasses, including As2S3, that typically
tion of As(V) and S2O23 with strain ANA-3, as measured by As2S3 exhibit hole conduction; this is in contrast to crystalline As2S3
absorption at 375 nm (Fig. S5). In other words, bacterial synthesis where electrons are more mobile [55,56]. 24% of the FETs demon-
of nanofibers was faster and more effective than the abiotic strated the reverse characteristics of increased conductance at
precipitation of already reduced As and S. These results indicate Vg > 0; this behavior is explained by the accumulation of electrons
that, beyond an active role in reduction, Shewanella cells play an in n-type nanofibers as the bands (bent down at the nanofiber-
additional role in catalyzing the nucleation of nanofibers from metal interface) are lowered [31,34]. The heterogeneity of the
reduced As(III) and S2 . nanofibers, in terms of dopant type, may reflect the complexity
We observed a significant reaction yield with strain ANA-3; the of the bacterial growth medium containing multiple elements in
As2S3 precipitate reached >80% of the maximum theoretical yield addition to As and S (see Materials and methods section). While
of each incubation after 60 days (Fig. 4). This theoretical yield is any residual salt and nutrient content appears to be below the
estimated by considering that the original 5 mM arsenate can yield detection limit of EDS (0.1 wt.% [57]) as a result of the extensive
a maximum 2.5 mM of As2S3 per liter in excess S conditions, washing procedure (Section 2.2), it is possible that trace elements
and using the As2S3 molecular weight of 246 g mol 1, resulting in may impact the electronic properties. Specifically, the residual ele-
a maximum yield of 49.2 mg for each 80 ml incubation ments may be responsible for the observed n-type doping in a frac-
(0.62 mg ml 1). In addition to evaluating the overall precipitation tion of the tested As2S3 nanofibers, which are otherwise known to
yield, we characterized the nanofiber growth rates and precipita- exhibit p-type conduction intrinsically [55]. These observations
tion rates during active synthesis. Our in situ observations also raise the interesting prospect of ‘biological doping’ that may
(Fig. 3) revealed a decline in the growth rates of individual nanof- influence, or tune, the properties of the biogenic nanomaterials
ibers with increased incubation time (from 10 to 3 nm min 1 depending on the constituents of the growth medium.
over 5 h). This observation is consistent with a limitation brought In addition to the p-type and n-type behavior of individual
about by the diminishing concentration of reactants in solution, nanofibers, a number of devices exhibited more complex gate
namely As(III) and S2 , as they get incorporated into the nanofibers dependencies, such as the mixed behavior seen in Fig. S3A,B. This
over time. By measuring the temperature dependence of the pre- unusual gate dependence was explained by a close inspection of
cipitation in bulk cultures over time (Fig. 4), we were able to such devices at the electrode–fiber interface (Fig. S3C), revealing
describe the initial precipitation rates with simple thermally that the semiconducting channel consisted of a bundle of
372 I.R. McFarlane et al. / Acta Biomaterialia 13 (2015) 364–373

heterogeneous fibers. While the underlying reason for the bundling deposition were performed at the USC Center for Electron
of smaller fibers is not yet clear, this phenomenon partially Microscopy and Microanalysis, where John Curulli and Dr. Matt
explains the significant diversity of diameters (20–600 nm) Mecklenburg provided valuable assistance. We are also grateful
observed in our study, since smaller-diameter nanofibers may to Guang-Sin Lu and Prof. Jan Amend for help and access to the
coalesce into larger-diameter structures. IC/AFS system. Michael Qian and Brian Zukotynski provided assis-
It should be noted that no effort was made to improve the tance in overnight UV–vis measurements. M.E.-N. acknowledges
overall device performance by annealing, which may further support from NASA through the NASA Astrobiology Institute under
decrease both the nanofiber and nanofiber–electrode contact resis- cooperative agreement NNA13AA92A.
tances, since our primary goal was to assess the as-synthesized
nanomaterials. From the transconductance of the NF-FETs, we Appendix A. Figures with essential colour discrimination
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 Certain figures in this article, particularly Figs. 4, 5, 7, 9 and 10
and n-type nanofibers, respectively. The p-type mobility is in are difficult to interpret in black and white. The full colour images
excellent agreement with the previously observed hole mobility can be found in the on-line version, at http://dx.doi.org/10.1016/
(10 4–10 5 cm2 V 1 s 1) in amorphous As2S3 glasses [55,56]. The j.actbio.2014.11.005.
biogenic NF-FET mobility demonstrated here is significantly lower
than many well-studied FETs based on crystalline or organic semi-
conductors [34,58]. While this results in small (pA) on currents and Appendix B. Supplementary data
on/off current ratios, it should be noted that the p-type devices
showed attractive threshold voltages (Vg  0 V). Future applica- Supplementary data associated with this article can be found, in
tions may also rely on the 2.37 eV optical band gap of the biogenic the online version, at http://dx.doi.org/10.1016/j.actbio.2014.
As2S3, which compares well to the 2.42 eV band gap of CdS, a tech- 11.005.
nologically important chalcogenide widely used in commercial
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