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Intrinsic electrical properties of cable bacteria reveal an Arrhenius temperature dependence


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Abstract Filamentous cable bacteria exhibit long-range electron transport over centimetre-scale distances, which takes place in a parallel fibre structure with high electrical conductivity. Still, the underlying electron transport mechanism remains undisclosed. Here we determine the intrinsic electrical properties of the conductive fibres in cable bacteria from a material science perspective. Impedance spectroscopy provides an equivalent electrical circuit model, which demonstrates that dry cable bacteria filaments function as resistive biological wires. Temperature-dependent electrical characterization reveals that the conductivity can be described with an Arrhenius-type relation over a broad temperature range (− 195 °C to + 50 °C), demonstrating that charge transport is thermally activated with a low activation energy of 40–50 meV. Furthermore, when cable bacterium filaments are utilized as the channel in a field-effect transistor, they show n-type transport suggesting that electrons are the charge carriers. Electron mobility values are ~ 0.1 cm2/Vs at room temperature and display a similar Arrhenius temperature dependence as conductivity. Overall, our results demonstrate that the intrinsic electrical properties of the conductive fibres in cable bacteria are comparable to synthetic organic semiconductor materials, and so they offer promising perspectives for both fundamental studies of biological electron transport as well as applications in microbial electrochemical technologies and bioelectronics.
FET measurements reveal an n-type semiconductor behaviour when fibre sheaths are used as the channel. (A) Transfer characteristics of a fibre sheath measured at a constant VDS\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${V}_{DS}$$\end{document}= 0.05 V (20 °C) show a modulation of the drain current ID\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${I}_{D}$$\end{document} when the gate bias VGS\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${V}_{GS}$$\end{document} is changed from 0 to 80 V to − 80 V and back to 0 V. The inset shows a fibre sheath to be a flattened ~ 150 nm double stack of fibres contained in a thin sheath. (B) Output characteristics of a fibre sheath under a constant gate voltage varying from − 50 to + 50 V in steps of 20 V show the slope of the current–voltage curve to change as a function of gate bias VGS\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${V}_{GS}$$\end{document}.
Temperature-dependent electrical characterization shows thermally activated charge transport. (A) The conductivity σ\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\sigma$$\end{document} of intact filaments and fibre sheaths show a linear relation with the inverted thermal energy 1/kT\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$1/{kT}$$\end{document}, thus following an Arrhenius behaviour with activation energy in the range of 40–50 meV. (B) Independent measurements of the impedance response as a function of temperature confirm this result. The similarity in the semicircle for every temperature implies the thermal activation only to be present in the (bulk) parallel resistance. (C) When fitted to an (RC) circuit, the parallel resistance Rp\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${{R}}_{{p}}$$\end{document} shows a similar thermal activation as found in (A), while the capacitance Cp\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$${C}_{{p}}$$\end{document} remained constant as a function of temperature.
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Scientic Reports | (2020) 10:19798 |
Intrinsic electrical properties
of cable bacteria reveal
an Arrhenius temperature
Robin Bonné1, Ji‑Ling Hou1, Jeroen Hustings1, Koen Wouters1, Mathijs Meert1,
Silvia Hidalgo‑Martinez2, Rob Cornelissen1, Filippo Morini1, Soe Thijs3, Jaco Vangronsveld3,4,
Roland Valcke5, Bart Cleuren6, Filip J. R. Meysman2,7 & Jean V. Manca1*
Filamentous cable bacteria exhibit long‑range electron transport over centimetre‑scale distances,
which takes place in a parallel bre structure with high electrical conductivity. Still, the underlying
electron transport mechanism remains undisclosed. Here we determine the intrinsic electrical
properties of the conductive bres in cable bacteria from a material science perspective. Impedance
spectroscopy provides an equivalent electrical circuit model, which demonstrates that dry cable
bacteria laments function as resistive biological wires. Temperature‑dependent electrical
characterization reveals that the conductivity can be described with an Arrhenius‑type relation over
a broad temperature range (− 195 °C to + 50 °C), demonstrating that charge transport is thermally
activated with a low activation energy of 40–50 meV. Furthermore, when cable bacterium laments
are utilized as the channel in a eld‑eect transistor, they show n‑type transport suggesting that
electrons are the charge carriers. Electron mobility values are ~ 0.1 cm2/Vs at room temperature
and display a similar Arrhenius temperature dependence as conductivity. Overall, our results
demonstrate that the intrinsic electrical properties of the conductive bres in cable bacteria are
comparable to synthetic organic semiconductor materials, and so they oer promising perspectives
for both fundamental studies of biological electron transport as well as applications in microbial
electrochemical technologies and bioelectronics.
In 2012, a novel group of filamentous bacteria was discovered1, which thrive in marine and freshwater
sediments2,3. From the analysis of the sediment chemistry, it was proposed that they can transport electrical
currents over centimetre distances1,4. ese so-called cable bacteria form unbranched chains of over 10,000 cells
that vertically orient in the sediment to take advantage of the redox gradients that occur in natural sediment
(Fig.1A,B)2. Metabolic oxidation and reduction reactions occur in dierent parts of the lament, and to ensure
the electrical coupling of these redox half-reactions, electrons are transported over centimetre-scale distances
along the lament1.
Direct electrode measurements reveal that individual cable bacterium laments can guide electrical currents
over distances up to 1cm under an externally applied potential5. is length scale of conduction for a single
organism surpasses greatly that of other known current-producing bacteria, such as Geobacter sulfurreducens and
Shewanella oneidensis MR-1. ese organisms form conductive nanowires that are a few micrometres long, and
act as model organisms in the eld of electromicrobiology6,7. e conductive structures that enable the long-range
transport in cable bacteria have recently been disclosed. Microscopy investigations reveal that all cells within a
cable bacterium lament share a common space within the cell envelope, and that a network of parallel bres
run within this periplasmic space along the whole lament8,9. ese periplasmic bres comprise the primary
1X-LAB, Hasselt University, Agoralaan D, 3590 Diepenbeek, Belgium. 2Department of Biology, University of
Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium. 3Centre for Environmental Sciences, Hasselt University,
Agoralaan D, 3590 Diepenbeek, Belgium. 4Department of Plant Physiology, Faculty of Biology and Biotechnology,
Maria Curie-Sklodowska University, Plac Marii Skłodowskiej-Curie 5, 20-400 Lublin, Poland. 5Molecular and
Physical Plant Physiology, Hasselt University, Agoralaan D, 3590 Diepenbeek, Belgium. 6Theory Laboratory,
Hasselt University, Agoralaan D, 3590 Diepenbeek, Belgium. 7Department of Biotechnology, Delft University of
Technology, Van der Maasweg 9, 2629HZ Delft, The Netherlands. *email:
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Scientic Reports | (2020) 10:19798 |
conductive structures of cable bacteria, forming an ordered and fail-safe network10 with conductivities up to
79 S/cm5 (Fig.1A). Nevertheless, the underlying electron transport mechanism remains currently undisclosed.
To gain fundamental insight into the long-range electron transport of cable bacteria, we have investigated
the intrinsic electrical properties of individual laments that were isolated from sediment enrichments. Using
a variety of electrical characterization techniques, we studied dried intact laments as well as so-called “bre
sheaths”, i.e. laments from which the lipid membranes and internal cytoplasm are removed by chemical extrac-
tion, thus retaining a sheath structure that embeds the conductive bres5,9(Fig.1A). tted to an (RC) circuit, the
parallel resistance (DC) and alternating current (AC) measurements to determine the intrinsic conductivity and
the inuence of contact resistances. Furthermore, the tunability of the transport was examined in a eld-eect
transistor set-up, which enables us to determine the charge carrier mobility. Finally, we employed the same
techniques in a cryostat set-up to study the conductivity and mobility as a function of temperature.
Cable bacteria act as resistive biological wires. In order to study the intrinsic electrical properties of
cable bacteria, it is crucial to unravel the electrical equivalent circuit and the inuence of contacts on the overall
electrical response. Previous measurements5 have produced linear current/voltage (IV) curves for both indi-
vidual intact laments and bre sheaths. Since these experiments were performed for a restricted voltage range
(− 0.1 to 0.1V), in this work we repeated them for larger voltage ranges (− 1 to 1V and − 10 to 10V). Measure-
ments were conducted in a probe stage set-up with gold, silver and carbon electrodes, and to minimize degrada-
tion of the conductive structures under the inuence of oxygen5, measurements were always performed under a
nitrogen atmosphere. Regardless of the voltage range, we consistently observed the same straight IV behaviour
(Fig.S1), which excludes that Schottky barriers are present at the lament/electrode interface and proving the
ohmic nature of these contacts.
To obtain a representative equivalent electrical circuit for cable bacteria, we performed electrical impedance
spectroscopy, where an AC voltage with varying frequency (range from 1Hz to 1MHz; amplitude 0.1V) is
applied to a single lament in the probe stage conguration. Individual laments were isolated from sediment
enrichments and used either as an intact lament (number of samples n = 6) or as a bre sheath (n = 4). Filaments
were positioned between two gold electrodes on glass or SiO2 substrates with a non-conductive interspacing
(100 to 500µm) (Fig.1C). Carbon paste was added at both ends to ensure a good electrical connection between
laments and gold electrodes (Fig. S2). All samples showed a similar response to the impedance measure-
ments, providing a semicircle in the complex impedance plane (Fig.2A,B). is behaviour can be described by
an equivalent electrical circuit that contains two serial resistors (
) of which one is in parallel with a
capacitor11 (Fig.2C). From a reference measurement where no lament was placed between the electrodes, an
equivalent circuit is obtained that does not include the resistance
), showing that the components
are inherent to the measurement setup, while
is attributed to the lament. e equivalent electri-
cal circuit is hence interpreted as follows: the series resistance
represents the combination of the resistance
of the measurement system wires and the resistance of the probe-electrode interface, while the capacitance
is attributed to the capacitance of the electrodes and the measurement system. e parallel resistance
comprises both the bulk resistance of the cable bacterium lament
and the contact resistance between the
electrodes and the lament
Values for
range from 0.8 MΩ to 3.6 GΩ (TableS1), corresponding with previously reported conduc-
tivity values5. Moreover, as expected,
is equal in value to the total resistance of the sample measured in a
Figure1. Electrical measurement set-ups for cable bacterium laments. (A) A graphical representation
of a cable bacterium with a set of parallel conductive bres in the cell envelope. Filaments for electrical
measurements are prepared either as intact laments or as a bre sheath aer removal of the cytoplasm
and membranes. (B) A SEM image of an intact cable bacterium shows the cells and ridges going along the
lament. (C) e lament is positioned between two electrodes on a non-conductive substrate for DC or AC
measurements. (D) In the FET measurements, two gold electrodes act as source S and drain D, while the highly
n-doped silicon gate electrode G imposes the eld eect at the bottom.
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subsequently performed DC measurement. Values for the other parameters were found to be
Cp=34 ±15
pF. e ratio
/Rp=0.004 ±0.008%
is consistently small, which aligns with the expected low
resistance of the measurement system connections. Over the broad range of experimental conditions examined,
which include dierent lament types (intact laments and bre sheaths), dierent lament lengths, a range
of lament conductivities as well as dierent electrode substrates, impedance results always showed a single
semicircle with no distinguishable other components in parallel with the system capacitance
. In order to
, an additional DC measurement as a function of distance was performed (see Fig.S2 and
TableS2), yielding a signicantly smaller value compared to
Overall, the obtained equivalent electrical circuit thus demonstrates that cable bacterium laments can be
considered as biological resistive wires with purely ohmic behaviour.
Transistor measurements show n‑type charge transport with high mobility. To determine the
magnitude of the charge carrier mobility, we examined laments in a eld-eect transistor (FET) conguration
(Fig.1D), where the inuence of an externally applied electric eld on the conduction is evaluated. In a bottom-
gate/bottom-contact FET conguration—as typically used to investigate the electrical properties of (in)organic
semiconductor lms—a single lament is placed across the source (S) and drain (D) electrodes separated by
various channel lengths (100 to 300µm) on top of a silicon dioxide/n-doped silicon gate (G) substrate. Since the
eld-eect is typically only present in a thin layer of the sample (~ 10–100nm) near the dielectric substrate, we
opted to work with bre sheaths, for which the distance between conductive bres and substrate is smaller than
for intact bacterial laments.
Transfer curves for a bre sheath are shown in Fig.3A. Here,
, and
represent the drain current,
gate-to-source voltage, and drain-to-source voltage, respectively. At zero gate bias (
= 0) and
= 0.1V,
the sample shows a high o-state
, which will be further discussed later on. With increasing positive gate bias
> 0) at 1V/s (other scan rates in Fig.S3),
slightly increases (about 9% at
= + 80V). In contrast, at
= − 80V,
decreases with 9%. is indicates that the charge density at the interface between bre sheath
and dielectric increases with increasing gate voltage, consistent with n-type semiconductor behaviour where
electrons are the maincharge carriers. To verify this, the leakage current
was monitored for all measurements
(n = 4), which was always more than two orders of magnitude smaller(1–10 pA) than the change in
Additionally, the output characteristics (
) were determined for
varying from − 50V to + 50V.
A typical graph is given in Fig.3B, where the gate bias modulates the linear slope (
) of the IV curve.
e conductivity linearly increases with gate bias
, yielding a modulation rate of 3 mS/cm per volt (Fig.S5).
Given the bias condition (
), the transistor response is found to be linear over the gate voltage
domain, as shown in Fig.3A. An estimate for the mobility of the electrons can be obtained by using the formula
µ=(∂ID/∂ VGS )·l/(w·VDS ·Ci)
in the linear bias mode condition at positive gate voltage, where
= 0.1–1mm
is the channel length and
= 4µm is a conservative estimate of the channel width12 since it corresponds to the
Figure2. e equivalent electrical circuit for an individual cable bacterium lament probed by impedance
spectroscopy. Nyquist plots of (A) intact laments and (B)bre sheaths show a similar single semicircle in the
complex plane. (C) e data were described as an equivalent electrical circuit consisting of a resistor Rs in series
with a parallel stack of a capacitor Cp and resistor Rp, comprising the cable bacterium RBulk and its contact with
the electrode RContact.
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width of the total bre sheath.
is the gate capacitance per unit area and can be calculated as
, with
the substrate oxide thickness,
the vacuum permittivity and
the relative dielectric permittivity of the gate
insulator. For the four bre sheaths examined, the electron mobility was found to be in the range of 0.09–0.27
cm2/Vs (TableS3), which is in the same order of magnitude as many organic semiconductors13.
Conduction is thermally activated with low activation energy over a wide temperature
range. To further understand the charge transport mechanism1416 in cable bacteria, we studied the con-
ductivity at dierent temperatures for a broad temperature range in a helium atmosphere (see “Methods” sec-
tion). Figure4A shows the conductivity
(see “Materials and Methods”) as a function of the inverted thermal
, for both an intact lament and a bre sheath, when cooled down in discrete steps from + 50°C
Figure3. FET measurements reveal an n-type semiconductor behaviour when bre sheaths are used as the
channel. (A) Transfer characteristics of a bre sheath measured at a constant
=0.05V (20°C) show a
modulation of the drain current
when the gate bias
is changed from 0 to 80V to − 80V and back to 0V.
e inset shows a bre sheath to be a attened ~ 150nm double stack of bres contained in a thin sheath. (B)
Output characteristics of a bre sheath under a constant gate voltage varying from − 50 to + 50V in steps of 20V
show the slope of the current–voltage curve to change as a function of gate bias
Figure4. Temperature-dependent electrical characterization shows thermally activated charge transport.
(A) e conductivity
of intact laments and bre sheaths show a linear relation with the inverted thermal
, thus following an Arrhenius behaviour with activation energy in the range of 40–50meV. (B)
Independent measurements of the impedance response as a function of temperature conrm this result. e
similarity in the semicircle for every temperature implies the thermal activation only to be present in the
(bulk) parallel resistance. (C) When tted to an (RC) circuit, the parallel resistance
shows a similar thermal
activation as found in (A), while the capacitance
remained constant as a function of temperature.
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to − 195°C. Both lament types demonstrate a similar behaviour; the conductance decreases with decreasing
temperature, thereby excluding the possibility of metal-like conduction. e activation energy
is determined
by tting the data with the Arrhenius function
17 (Fig.4A). e tted curves show similar
slopes, indicating comparable activation energies; the dierences in osets indicate a dierent room temperature
conductivity as observed before. Heating the samples back from − 195 to + 50°C resulted in similar activation
energy, thereby demonstrating any lament decay to be small (Fig. S6). An average of the activation energy for
all samples (TableS4) results in 42.3 ± 6.5meV for intact laments (n = 8) and 48.4 ± 7.4meV for bre sheaths
(n = 10)—very close to the room temperature
value of 25meV and low compared to typical activation ener-
gies in the order of 500meV for biological conductors16 like S. oneidensis nanowires18. is result demonstrates
that electron transport in cable bacteria is thermally activated, and laments remain conductive far beyond the
natural physiological temperature range of living cable bacteria.
To verify whether the low activation energy is intrinsic, the impedance response was measured as a func-
tion of temperature in a new set of experiments. Figure4B shows a complex plane plot for an intact lament for
temperatures ranging from − 175 to + 50°C (n = 3). Again we deduce for all temperatures a similar semicircle as
shown in Fig.4B, showing a negligible system resistance
. is time, the equivalent circuit (
) was tted to
the data (TableS5). e
value agrees well with the corresponding DC value, and a similar Arrhenius behaviour
is found with a corresponding activation energy
= 40.1 ± 5.3meV, while
was found to be constant over the
whole temperature range (Fig.4C).
Temperature‑dependent FET measurements show a similar thermally activated mobility. In
order to further unravel the electron transport mechanism, the FET characteristics are likewise studied as a
function of temperature for the same range of − 195°C to + 50°C, with smaller increments. Fibre sheath samples
were prepared as before and laid on interdigitated gold electrodes (10 lines, interspacing 20µm) to enhance the
current signal at low temperatures. For a series of 30 dierent temperatures, a transfer curve is made. As shown
in Fig.5A, the transfer curves at low temperature more resemble a classical n-type FET behaviour as compared
to room temperature (Fig.3A), with a higher change in
at positive gate voltages and almost no eect at nega-
tive gate voltages.
e mobility was calculated from a t over the positive gate voltages, again using the linear mode bias condi-
tion. In Fig.5B the calculated mobility is plotted as a function of temperature. At temperatures above − 100°C
(I.E. the le part of the graph), the retrieved mobility values show more variation, which is attributed to a less pro-
nounced transistor response at those temperatures (see also the “Discussion”). An Arrhenius behaviour becomes
apparent over the temperature range of − 195°C to − 100°C. When tting the data to the Arrhenius relationship
, similar activation energy for the mobility as for the conductivity can be determined. Aver-
aged over n = 3 measurements (TableS6), the activation energy for the electron mobility is 36 ± 5meV, compared
to a value for the activation energy of conductivity of 50 ± 2meV, measured on the same samples.
In this work, we report the intrinsic electrical properties of dry cable bacterium laments with dierent char-
acterization techniques. Using electrical impedance spectroscopy, we found a single semicircle in the complex
plane, indicating that cable bacteria can be considered as biological electrical wires with ohmic contacts. ese
results are in line with a theoretical impedance analysis for transport in stochastic systems19, but also correspond
toGeobacter nanowires20,21 with the exclusion of an ionic component to the overall conductivity.
Alongside a high electrical conductivity (> 10 S/cm;6 and this work), our results demonstrate that the con-
ductive bres in the cell envelope of cable bacteria display high electron mobility (10–1 cm2/Vs) for a biological
material. ese values are similar in magnitude to organic semiconducting nanowires13,22,23 like P3HT24 and
PEDOT:PSS25 and close to the charge carrier mobility in amorphous silicon (1 cm2/Vs)22. Furthermore, the
Figure5. e electron mobility of the conductive structures in cable bacteria is thermally activated. (A) A
transfer characteristic at lower temperature (at a constant
=0.5V) indicates the n-type eect is more
prominent at lower temperatures. Calculated from transfer curves at dierent temperatures, (B) the mobility
is plotted as a function of temperature to reveal that the electron mobility is thermally activated, following an
Arrhenius relationship for temperatures below -100°C.
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estimated charge carrier mobility is higher than that of nanowires from G. sulfurreducens (10–4 to 10–2 cm2/Vs)26,27
and comparable to the hole mobility of the conductive structures of S. oneidensis (10–1 cm2/Vs)28. e promis-
ing values for the mobility for the conductive structures in cable bacteria make them an interesting candidate
material in the search for organic and biological alternatives to classical semiconductors. Furthermore, cable
bacteria show a transistor response that is detectable over a broad voltage range, though with a smaller eect
as compared to Geobacter20 and Shewanella nanowires28, but becoming more apparent at lower temperatures.
is limited tunability may be at least in part due to the particular geometric conguration of the bre sheaths
examined here. e conductive bres are embedded in a non-conductive matrix, and only the bottom layer of
the ~ 120nm double stacked bres is expected to be inuenced by the gate electric eld9, while the upper layer
will act as a temperature dependent conductive pathway, which will disturb the transistor behaviour at higher
temperatures (Fig.4A, inset). For individually isolated bres, we expect a higher tunability.
Our temperature-dependent experiments reveal that the conductivity and electron mobility is thermally
activated and can be described by an Arrhenius relation with an activation energy of around 45meV. Arrhenius
behaviour has also been found for thin lms of proteins and peptides placed between planar electrodes15,16,
as well as in inorganic nanowires with surface defects29,30, and is commonly attributed to (multistep) hopping
transport. However, where a multistep hopping transport is proposed for S. oneidensis nanowires6, the charge
transport mechanism in G. sulfurreducens nanowires remains unclear and under debate21,3133. Future structural
and electrical studies are needed to elucidate the electrical transport mechanism inside the periplasmic bres
of cable bacteria and distinguish between multistep hopping26,33, variable range hopping34, coherence assistant
hopping, or other mechanisms30,35.
e electrical properties of cable bacteria described here oer new perspectives not only for fundamental
studies, but also for technological applications. Our observations that cable bacteria can function as electrical
interconnections with low contact resistance, as well as active electrical channels in FETs, show that they can be
envisioned as suitable future materials for the emerging eld of bioelectronics36, including visionary technolo-
gies such as biodegradable electronics. e reported intrinsic electrical properties, together with the long-range
electron transport and the wide temperature range of operation, are unique assets to envisage cable bacteria for
these future electronic applications.
Materials and methods
Sample preparation. Cable bacteria were enriched in natural sediment cores incubated in oxygenated
seawater, as described previously3. Sediment was collected at Rattekaai (Oosterschelde, e Netherlands). Single
laments of cable bacteria were picked from the sediment enrichment, as described previously9. Filaments were
washed at least six times in MilliQ water to remove sediment debris, thus providing so-called “intact laments.
Any excess of water was removed with a pipette and the sample was le to dry. Overall, about 5min passed
between the picking of a lament and the start of the current measurement. Alternatively, aer washes with Mil-
liQ, laments were exposed to a sequential extraction procedure, thus removing the cytoplasm and membranes,
as described previously9. is provided so-called bre sheaths. Aer about 45min of preparation time, the sam-
ple was transferred onto the electrode substrate.
AC/DC electrical measurements. For all electrical measurements, the substrate was placed at a probe
station with two needle probes connecting to the two electrodes. e probe stage is housed in a nitrogen glove-
box to prevent sample decay. In the DC measurements, the probe station was connected to a Keithley 2450A
sourcemeter (Keithley, USA) with triax cables, driven by the multi-tool control soware SweepMe, as described
earlier5. For AC impedance measurements, the sample is probed with a VersaSTAT3F potentiostat (Ametek,
USA), allowing impedance measurements in the range 1MHz to 1Hz or 100mHz at bias voltage 0.1V. ese
results were veried with a MFIA impedance analyser (Zurich Instruments, Switzerland) for frequencies in the
range of 5MHz to 1Hz. Data tting was done with both the ZSimpWin and ZView soware packages (Solartron,
USA). Conductivity
was calculated for all samples using
, with
the conduction length,
= 0.12 µm2
the conductive area (about 60 bres of 50nm diameter)9 and
the conductance calculated with a
linear t to the IV-diagrams.
Field‑eect transistor measurements. Field-eect measurements were done on a highly n-doped sili-
con wafer in a bottom-gate bottom-contact FET conguration. A 150nm thick thermally grown silicon oxide
layer served as a dielectric layer, and the bottom drain and source gold electrodes with a thickness of 50nm of
the coplanar FET were dened by optical lithography to yield a channel length of 100µm. Aer the washing
and extraction treatments, as mentioned above, an individual lament was placed across the source and drain
contacts. Gate-source and drain-source voltages were applied by two separate Keithley 2450A sourcemeters, for
which the current response was continuously monitored.
e time response of the drain current upon applying a positive gate bias depends on the time to build up the
conductive channel. erefore, in order to measure consistent transfer curves, a proper gate sweeping speed was
crucial. Fig.S3 shows the transfer curves measured at a gate sweeping speed varying from 10, 2, 1, and 0.5V/s.
Using a fast scanning speed of 10V/s, the signal of
shows a large hysteresis. Stable
is obtained by reducing
the gate sweeping speed down to 2V/s and 1V/s.
Temperature‑dependent measurements. Temperature measurements were performed in two dier-
ent cryostats. Initial DC measurements were performed with a commercial model OptistatDN by Oxford Instru-
ments. e cryostat is liquid nitrogen-based, allowing the sample to be cooled down from ambient temperature
to − 195°C. Cable bacterium laments were dropcasted on glass substrates, and carbon paste was applied to both
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Scientic Reports | (2020) 10:19798 |
ends to form electrical contact points. ese were mounted in a double-walled cryostat using spring contacts.
e inner vessel was lled with helium as exchange gas, the outer vessel by a high vacuum, maintaining a pres-
sure around 10–9bar for thermal insulation. e sample was heated to 50°C and then cooled down to − 195°C in
steps of 25°C. For each step, current–voltage curves were measured to obtain the conductivity
. Cooling down
was achieved by adjustment of a needle valve for the liquid nitrogen ow towards the heat-exchanger. A steady-
state temperature is established by the combination of the heat exchanger and an adjacent heating element. e
latter was coupled in a feedback loop to a temperature control unit, model ITC 502 by Oxford Instruments. Aer
stabilization of the current (about 15min), a current–voltage measurement was performed at each temperature.
For temperature-dependent AC and FET measurements, and as verication experiments of the previous
set-up, a cryostat probe stage HFS350EV-PB4 with liquid nitrogen pump LNP96-S and LINK soware was used
(Linkam, UK). Coax outlets were coupled to the MFIA or adapted to triax cables to connect to the Keithley
2450A sourcemeters. e prepared sample is loaded on the stage and purged with nitrogen gas for 3min. It
was then cooled down to − 195°C with liquid nitrogen in the disk underneath the sample. In steps of 25°C
or smaller, the sample is heated to 50°C. e current was monitored to stabilize (aer 1 to 5min) before the
characterization measurement was performed. For AC measurements, a bias voltage of 300mV was applied;
for FET measurements
was chosen to enhance the current output signal. Aer the measurements, all
samples were studied with an optical microscope to verify if there was no degradation or damage due to cooling
to low temperatures.
Statistics. All measurements were at least performed in triplicates. e value “n” in the text symbolizes the
number of samples, and averages are given
the standard deviation.
Received: 28 August 2020; Accepted: 30 October 2020
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e authors thank the colleagues from X-LAB from Hasselt University and the Microbial Electricity team from
the University of Antwerp for discussions and feedback. Special thanks to K. Ceyssens and T. Custers for the
graphics in Fig.1A; R. Lempens and M. De Roeve for help with the experimental set-up; J. D’Haen for SEM
imaging (Fig.1B). Graphics for Fig.1C,D and Fig.3A were made by RB with Adobe illustrator. is research was
nancially supported by the Research Foundation—Flanders (FWO project grant G031416N to FJRM and JM
and FWO aspirant grant 1180517N to RB). FJRM was additionally supported by the Netherlands Organization
for Scientic Research (VICI grant 016.VICI.170.072).
Author contributions
Impedance and contact resistance measurements were performed by R.B.; transistor measurements by R.B.,
J.L.H. and M.M.; cryostat measurements by R.B., J.L.H., K.W. and J.H.; SEM measurements by J.D. Cable bacte-
ria cultivation and sample preparation were done by S.H.M., R.B., J.L.H. and F.J.R.M. e study was conceived
by J.M. Furthermore, R.C., S.T., F.M., J.V., R.V., F.J.R.M. and B.C. contributed to discussions and preparation of
the manuscript.
Competing interests
e authors declare no competing interests.
Additional information
Supplementary information is available for this paper at https:// doi. org/ 10. 1038/ s41598- 020- 76671-5.
Correspondence and requests for materials should be addressed to J.V.M.
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... 48 Copyright 2018 Elsevier Ltd. (C) Illustration depicting cable bacteria possessing parallel conductive fibers in their cell envelope. Adapted with permission from Bonnéet al. 49 Copyright 2020 Springer Nature. (D) Scheme highlighting the extracellular electron transport (EET) and long-distance electron transport in cable bacteria. ...
... 50 This air sensitivity, in addition to n-type transport when used as channel material for field effect transistors, is consistent with electrons being the main charge carriers. 49,50 Electrical measurements revealed that electron transport is thermally activated with low activation energy (40−50 meV) and electron mobility of 10 −1 cm 2 V −1 s −1 , comparable with the average mobility of many n-type organic semiconductors. 49,271 The conductivities reported here are much higher than undoped OSC films. ...
... 49,50 Electrical measurements revealed that electron transport is thermally activated with low activation energy (40−50 meV) and electron mobility of 10 −1 cm 2 V −1 s −1 , comparable with the average mobility of many n-type organic semiconductors. 49,271 The conductivities reported here are much higher than undoped OSC films. FET measurements of individual cable bacterium filaments show the field effect electron mobility up to 0.27 cm 2 /(V s). ...
... The cable aging is simulated in normal aging condition in this research, so that the cable degradation condition can be directly related to its actual insulation age. The accelerated aging time should be converted into normal aging time according to the Arrhenius law [22], which can be represented as: ...
... This teaming up with complementary techniques is essential since ToF-SIMS can provide insights on the chemical composition of cable bacteria, but is not a quantitative technique and therefore does not allow to quantify Ni and S density. In our recent work on the intrinsic electrical properties of cable bacteria, we have observed an Arrhenius-type relation for the temperature dependence of the electrical conductivity and electron mobility over a broad temperature range (-195°C to +50°C), demonstrating that charge transport is thermally activated 30 . ...
Biology leverages a range of electrical phenomena to extract and store energy, control molecular reactions and enable multicellular communication. Microbes, in particular, have evolved genetically encoded machinery enabling them to utilize the abundant redox-active molecules and minerals available on Earth, which in turn drive global-scale biogeochemical cycles. Recently, the microbial machinery enabling these redox reactions have been leveraged for interfacing cells and biomolecules with electrical circuits for biotechnological applications. Synthetic biology is allowing for the use of these machinery as components of engineered living materials with tuneable electrical properties. Herein, we review the state of such living electronic components including wires, capacitors, transistors, diodes, optoelectronic components, spin filters, sensors, logic processors, bioactuators, information storage media and methods for assembling these components into living electronic circuits.
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The global production of unrecycled electronic waste is extensively growing each year, urging the search for alternatives in biodegradable electronic materials. Electroactive bacteria and their nanowires have emerged as a new route toward electronic biological materials (e-biologics). Recent studies on electron transport in cable bacteria—filamentous, multicellular electroactive bacteria—showed centimeter long electron transport in an organized conductive fiber structure with high conductivities and remarkable intrinsic electrical properties. In this work we give a brief overview of the recent advances in biodegradable electronics with a focus on the use of biomaterials and electroactive bacteria, and with special attention for cable bacteria. We investigate the potential of cable bacteria in this field, as we compare the intrinsic electrical properties of cable bacteria to organic and inorganic electronic materials. Based on their intrinsic electrical properties, we show cable bacteria filaments to have great potential as for instance interconnects and transistor channels in a new generation of bioelectronics. Together with other biomaterials and electroactive bacteria they open electrifying routes toward a new generation of biodegradable electronics.
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Cable bacteria are an emerging class of electroactive organisms that sustain unprecedented long‐range electron transport across centimeter‐scale distances. The local pathways of the electrical currents in these filamentous microorganisms remain unresolved. Here, the electrical circuitry in a single cable bacterium is visualized with nanoscopic resolution using conductive atomic force microscopy. Combined with perturbation experiments, it is demonstrated that electrical currents are conveyed through a parallel network of conductive fibers embedded in the cell envelope, which are electrically interconnected between adjacent cells. This structural organization provides a fail‐safe electrical network for long‐distance electron transport in these filamentous microorganisms. The observed electrical circuit architecture is unique in biology and can inspire future technological applications in bioelectronics. Long before the age of microelectronics, a group of filamentous microorganisms named cable bacteria developed an electrical network within their own cell structure. In this work, the local electrical pathways for cable bacteria are revealed using conductive atomic force microscopy, showing a fail‐safe electrical structure conducted by parallel and electrically interconnected biological fibers.
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Biological electron transport is classically thought to occur over nanometre distances, yet recent studies suggest that electrical currents can run along centimetre-long cable bacteria. The phenomenon remains elusive, however, as currents have not been directly measured, nor have the conductive structures been identified. Here we demonstrate that cable bacteria conduct electrons over centimetre distances via highly conductive fibres embedded in the cell envelope. Direct electrode measurements reveal nanoampere currents in intact filaments up to 10.1 mm long (>2000 adjacent cells). A network of parallel periplasmic fibres displays a high conductivity (up to 79 S cm(-1)), explaining currents measured through intact filaments. Conductance rapidly declines upon exposure to air, but remains stable under vacuum, demonstrating that charge transfer is electronic rather than ionic. Our finding of a biological structure that efficiently guides electrical currents over long distances greatly expands the paradigm of biological charge transport and could enable new bio-electronic applications.
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Cable bacteria are long, multicellular micro-organisms that are capable of transporting electrons from cell to cell along the longitudinal axis of their centimeter-long filaments. The conductive structures that mediate this long-distance electron transport are thought to be located in the cell envelope. Therefore, this study examines in detail the architecture of the cell envelope of cable bacterium filaments by combining different sample preparation methods (chemical fixation, resin-embedding, and cryo-fixation) with a portfolio of imaging techniques (scanning electron microscopy, transmission electron microscopy and tomography, focused ion beam scanning electron microscopy, and atomic force microscopy). We systematically imaged intact filaments with varying diameters. In addition, we investigated the periplasmic fiber sheath that remains after the cytoplasm and membranes were removed by chemical extraction. Based on these investigations, we present a quantitative structural model of a cable bacterium. Cable bacteria build their cell envelope by a parallel concatenation of ridge compartments that have a standard size. Larger diameter filaments simply incorporate more parallel ridge compartments. Each ridge compartment contains a ~50 nm diameter fiber in the periplasmic space. These fibers are continuous across cell-to-cell junctions, which display a conspicuous cartwheel structure that is likely made by invaginations of the outer cell membrane around the periplasmic fibers. The continuity of the periplasmic fibers across cells makes them a prime candidate for the sought-after electron conducting structure in cable bacteria.
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The conduction of ions and electrons over multiple length scales is central to the processes that drive the biological world. The multidisciplinary attempts to elucidate the physics and chemistry of electron, proton, and ion transfer in biological charge transfer have focused primarily on the nano‐ and microscales. However, recently significant progress has been made on biomolecular materials that can support ion and electron currents over millimeters if not centimeters. Likewise, similar transport phenomena in organic semiconductors and ionics have led to new innovations in a wide variety of applications from energy generation and storage to displays and bioelectronics. Here, the underlying principles of conduction on the macroscale in biomolecular materials are discussed, highlighting recent examples, and particularly the establishment of accurate structure–property relationships to guide rationale material and device design. The technological viability of biomolecular electronics and ionics is also discussed. Inspired by biological charge transfer, the field of biomolecular electronics has emerged. The ability of biomolecular macroscopic structures to mediate charge transport over millimeter and centimeter length scales, while differentiating between electron or ionic conduction, is explored, along with the different possible mechanisms of conduction. The most plausible applications for biomolecular macroscopic structures are also discussed.
Biological electron transfer (ET) is one of the most studied biochemical processes due to its immense importance in biology. For many years, biological ET was explained using the classical incoherent transport mechanism, i.e., sequential hopping. One of the relatively recent major observations in this field is long-range extracellular ET (EET), where some bacteria were shown to mediate electrons for extremely long distances on the micrometer length scales across individual nanowires. This fascinating finding has resulted in several suggested mechanisms that might explain this intriguing EET. Much recently, the structure of a conductive Geobacter sulfurreducens nanowire has been solved, which showed a highly ordered quasi 1-dimensional wire of a hexaheme cytochrome protein, named OmcS. Based on this new structure, we suggest here several electron diffusion models for EET, involving either purely hopping or several degrees of mixed hopping and coherent transport, in which the coherent part is due to a local rigidification of the protein structure, associated with a drop of the local reorganization energy. The effect is demonstrated for two closely packed heme sites as well as for longer chains containing up to several dozens porphyrins. We show that the pure hopping model probably cannot explain the reported conductivity values of the G. sulfurreducens nanowire using conventional values of reorganization energy and electronic coupling. On the other hand, we show that for a wide range of the latter energy values, the mixed hopping-coherent model results in a superior electron diffusion compared to the pure hopping model, and especially for long-range coherent transport, involving multiple porphyrin sites.
The effects of hydrogen and hydroxyl passivation on the structure, electrical and optical properties of SiCNWs were investigated. The passivation performance of different atoms (groups) were discussed by analyzing the distribution of electronic states and the polarity of chemical bonds. The results show that passivation can improve the stability of SiCNWs structure, and the effect of hydroxyl is better than hydrogen passivation. And hydrogen and hydroxyl passivation both increase the band gap of SiCNWs, and the changing trend of band gap is relevant to the polarity of the covalent bond formed by the passivation of surface atoms. Moreover, passivation enhances the stability of the optical properties of SiCNWs, resulting in narrowing of light absorption, photoconductivity and other spectra, and the response peak shifts to the deep ultraviolet region, which means that hydrogen or hydroxyl passivation of SiCNWs is likely to be a candidate material for deep ultraviolet micro-nano optoelectronic devices.
The concept of impedance, which characterises the current response to a periodical driving, is introduced in the context of stochastic transport. In particular, we calculate the impedance for an exactly solvable model, namely the stochastic transport of particles through a single-level quantum dot.
Long-range (>10 μm) transport of electrons along networks of Geobacter sulfurreducens protein filaments, known as microbial nanowires, has been invoked to explain a wide range of globally important redox phenomena. These nanowires were previously thought to be type IV pili composed of PilA protein. Here, we report a 3.7 Å resolution cryoelectron microscopy structure, which surprisingly reveals that, rather than PilA, G. sulfurreducens nanowires are assembled by micrometer-long polymerization of the hexaheme cytochrome OmcS, with hemes packed within ∼3.5–6 Å of each other. The inter-subunit interfaces show unique structural elements such as inter-subunit parallel-stacked hemes and axial coordination of heme by histidines from neighboring subunits. Wild-type OmcS filaments show 100-fold greater conductivity than other filaments from a ΔomcS strain, highlighting the importance of OmcS to conductivity in these nanowires. This structure explains the remarkable capacity of soil bacteria to transport electrons to remote electron acceptors for respiration and energy sharing.
Bioelectronic materials interface biomolecules, cells, organs, or organisms with electronic devices, and they represent an active and growing field of materials research. Protein and peptide nanostructures are ideal bioelectronic materials. They possess many of the properties required for biocompatibility across scales from enzymatic to organismal interfaces, and recent examples of supramolecular protein and peptide nanostructures exhibit impressive electronic properties. The ability of such natural and synthetic protein and peptide materials to conduct electricity over μm to cm length scales, however, is not readily understood from a conventional view of their amino acid building blocks. Distinct in structure and properties from solid state inorganic and synthetic organic metals and semiconductors, supramolecular conductive proteins and peptides require careful theoretical treatment and experimental characterization methods to understand their electronic structure. In this review, we discuss theory and experimental evidence from recent literature describing the long-range conduction of electronic charge in protein and peptide materials. Electron transfer across proteins has been studied extensively, but application of models for such short-range charge transport to longer distances relevant to bioelectronic materials are less well understood. Implementation of electronic band structure and electron transfer formulations in extended biomolecular systems will be covered in the context of recent materials discoveries and efforts at characterization of electronic transport mechanisms.
Significance Cable bacteria were recently discovered as the facilitators of electron transfer over centimeter distances in marine sediments. In this work, we explore the unique structure of the cable bacteria, using atomic force microscopy-based single-cell in vitro dissection. We identify different types of bacterial cell–cell junctions and continuous dimeric strings hidden under the outer membrane that pass through the cell junctions. The strings seem to serve an important function in maintaining the integrity of individual cable bacteria cells as a united filament. On the basis of our findings, we propose a model for the division and growth of the cable bacteria, which illustrate the possible structural requirements for the formation of centimeter-length filaments in the recently discovered cable bacteria.