Electron transfer through α-peptides attached to vertically aligned carbon nanotube arrays: A mechanistic transition

Article abstract of DOI:10.1039/c2cc16665h

The mechanism of electron transfer in α-aminoisobutyric (Aib) homoligomers is defined by the extent of secondary structure, rather than just chain length. Helical structures (Aib units ≥3) undergo an electron hopping mechanism, while shorter disordered sequences (Aib units <3) undergo an electron superexchange mechanism. The Royal Society of Chemistry 2012.

Full text of DOI:10.1039/c2cc16665h

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COMMUNICATION
Electron transfer through a-peptides attached to vertically aligned carbon
nanotube arrays: a mechanistic transitionwz
Jingxian Yu,a Ondrej Zvarec,a David M. Huang,a Mark A. Bissett,b Denis B. Scanlon,a
Joe G. Shapterb and Andrew D. Abell*a
Received 27th October 2011, Accepted 1st December 2011
DOI: 10.1039/c2cc16665h
The mechanism of electron transfer in a-aminoisobutyric (Aib)
homoligomers is defined by the extent of secondary structure,
rather than just chain length. Helical structures (Aib units Z 3)
undergo an electron hopping mechanism, while shorter disordered
sequences (Aib units o3) undergo an electron superexchange
mechanism.
SWCNTs/Si electrodes have previously been well charac-
terised using a range of techniques,21,23,24 and they are well
documented for use in electrochemical studies.20,21,25,26
The required peptides were prepared by N-acylating ferrocenyl-
methylamine with oligomers of a-aminoisobutyric acid (see
Fig. 1b and the ESIz). The conformations of these were
determined, by 2D-NMR spectroscopy, to be disordered and
310-helical for structures with n = 1–2 and n = 3–5 Aib units,
respectively. This is consistent with related structures.7,15 The
prepared oligomers were separately attached to a SWCNTs/Si
electrode prepared with an average nanotube separation (50 nm)
significantly larger than the length of the peptides (see Table 1)
in order to limit the possibility of electrochemical shortcuts (see
the ESIz). SWCNTs/Si functionalised with peptides containing
3, 4, and 5 Aib units gave IR absorptions at 1670 (amide I) and
1540 (amide II), which is consistent4,27 with a 310-helical
conformation on the surface (see the ESIz). Electrochemical
measurements of the immobilised oligopeptides (Fig. 1c) were
then carried out in 0.1 M TBAPF6/CH3CN solution using a
specially designed electrochemical cell,21 which provides a small
working area (B0.2 mm2) and tiny separation between working
and reference electrodes. The ohmic-drop corrected electro-
chemical data were analysed as for other related studies.13,28,29
The ability to transfer an electron from one biomolecule to
another is critical to key biological processes, including photo-
synthesis and respiration.1,2 This ‘flow of electrons’ is catalysed
by oxidoreductases over surprisingly large molecular distances
(4100 A).3,4 A number of factors influence the kinetics of this
process, including peptide chain length, dipole orientation and
hydrogen bonding.5–9 Of particular significance is the suggestion
that peptides can undergo electron transport via either a bridge-
assisted superexchange or electron hopping mechanism, depending
on the separation of electron donor and acceptor groups.2,10–13
However, the exact role that these and other factors play in
defining the mechanism is contentious.10–12 In this paper, we
present electrochemical evidence that the mechanism of electron
transfer through oligomers of a-aminoisobutyric acids (Aib) is
defined by secondary structure and associated intramolecular
hydrogen bonding. Oligomers of Aib were used in the study
since relatively short sequences (3 or more units) are known to
form predictable and particularly stable helical structures.14–16
The analysis was carried out by attaching the oligopeptides to
vertically aligned single-walled carbon nanotube arrays/silicon
electrodes (SWCNTs/Si, see Fig. 1a and the ESIz) to provide a
large surface area and rigid support for attachment, with excellent
electron communication between electrodes and peptides.17–22
a School of Chemistry and Physics, The University of Adelaide,
Adelaide, SA 5005, Australia. E-mail: andrew.abell@adelaide.edu.au;
Fax: (+61) 8 8303 4358; Tel: (+61) 8 8303 5652
b School of Chemical & Physical Science, Flinders University,
Bedford Park, SA 5042, Australia. E-mail: joe.shapter@flinders.edu.au;
Fax: (+61) 8 8201 2905; Tel: (+61) 8 8303 2005
w This article is part of the ChemComm ‘Artificial photosynthesis’ web
themed issue.
z Electronic supplementary information (ESI) available: General
information, synthesis of peptides, geometry of N-ferrocene-oligopetides,
preparation of SWCNTs/Si arrays, attachment of ferrocene-oligopeptide
to SWCNTs/Si arrays, characterisation of modified SWCNTs/Si arrays
with attached ferrocene-oligopeptides, electrochemistry, discussions on
the roles of SWCNT and Si surface in the electron transfer process. See
DOI: 10.1039/c2cc16665h
Fig. 1 Schematic of ferrocene-derivatised oligopeptide immobilised
SWCNT array/silicon electrode and its fabrication.
c
1132 Chem. Commun., 2012, 48, 1132–1134
This journal is The Royal Society of Chemistry 2012

Table 1 Electron transfer rate constants, apparent surface concen-
trations, formal potentials and iron-to-terminal nitrogen distances of
ferrocenylmethylamine and ferrocene-derivatised oligopetides
geometries obtained using the hybrid B3LYP method with
6-31G** basis set (see the ESIz).
The apparent surface concentrations (Table 1) are approx.
10 times greater than those obtained for peptides attached to
flat gold electrodes.27 This reflects the relative rough surface of
the nanotube array, which accommodates the binding of a
large amount of peptide.22 This leads to improved reliability
and reproducibility of the electrochemical response.21 A graph
(Fig. 3a) of electron transfer rate constant (kapp) vs. the iron-
to-terminal nitrogen distance (as defined by the number of
constituent monomers and secondary structure) reveals a clear
dependence between the two parameters. A slope transition is
observed on a change to structures containing more than two
a-aminoisobutyric acid units (see the last 3 points on this
graph). A similar transition has been demonstrated in DNA,28
peptide nucleic acid34 and polyproline-bridged systems.13
The structures that possess a well-defined helical conforma-
tion display a weak dependence of the electron transfer rate
constant on distance, as evidenced by the shallow slope in
Fig. 3a. This is consistent with a hopping mechanism.11,13,28,35
Aib Distance Surface concentration E0 (V vs.
(ꢁ10ꢀ10 mole cmꢀ2
No. (A)
)
SCE)
kapp (sꢀ1
)
0
1
2
3
4
5
4.36
5.37
6.39
9.93
12.30
14.12
4.86 ꢂ 0.45
7.91 ꢂ 0.81
6.22 ꢂ 0.57
2.04 ꢂ 0.19
4.68 ꢂ 0.43
2.15 ꢂ 0.21
0.503
0.486
0.481
0.475
0.463
0.458
745.5 ꢂ 56.4
341.3 ꢂ 29.1
136.8 ꢂ 16.3
93.4 ꢂ 9.2
72.1 ꢂ 5.6
63.2 ꢂ 4.3
A detailed calculation (see the ESIz) on each sequential step in
the overall electron transfer process in this system clearly
shows that the electron transfer rate in the peptides is at least
8 orders of magnitude slower than that for all other electron
transfer steps. Therefore we can safely ignore these other steps
in the analysis of electrochemical data.
The resulting cyclic voltammograms show a pair of redox
peaks with a significant non-faradaic background current
(Fig. 2a). Well-formed redox peaks are observed at approx.
450 mV for the surface attached ferrocene-derivatised oligo-
peptide (Fig. 2b, n = 5, i.e. Aib5-Fc) after background
subtraction. The non-faradaic background current is attributed
to capacitive effects associated with charging of the electrode/
electrolyte interface30 and was expected due to the rough
surface.25 The lack of a redox response from the control
experiment (no coupling agents used for the preparation of
control samples) excludes the possibility that the ferrocene-
capped peptides are physically adsorbed.20,25 The observed
straight-line relationship between the oxidation/reduction
currents and scan rate indicates that the electrode reaction
occurs via a surface bound species.31 This provides further
evidence that the observed electrochemical redox peaks are due
to the covalently anchored ferrocene-derivatised molecules.
The FWHM (Full-Width Half-Maxima, Fig. 2b) for both the
anodic and cathodic peaks are 160 and 150 mV respectively,
greater than the theoretical value of 90.6 mV (ferrocene
oxidation/reduction is a single electron process), indicating
an inhomogeneous chemical environment of the Fc compounds
on nanotubes.32 Electrochemical data analysis using Laviron’s
methodology33 (see the ESIz) gave the electron transfer rate
constants, surface concentrations, and formal potentials for ferro-
cenylmethylamine and the ferrocene-derivatised oligopeptides, as
summarised in Table 1. The table also contains iron-to-terminal
nitrogen distances for each structure, as determined by optimised
The rate attenuation constant (b) was estimated to be 0.10 Aꢀ1
.
A plot of the inverse of the square root of kapp vs. the iron-to-
terminal nitrogen distance (Fig. 3b) shows a straight line, which
provides further evidence for a hopping mechanism.4 The shorter
sequences gave rise to a steep decrease, which is consistent
with an alternative electron superexchange mechanism.2,3,11,13
The apparent rate attenuation constant (b) for these peptides
was calculated to be 0.84 Aꢀ1. These rate attenuation constants
are smaller than those reported for an oligoproline-bridge
Fig. 3 (a) Dependence of kapp on iron-to-terminal nitrogen distance.
(b) Plot of the inverse of the square root of kapp vs. the iron-to-terminal
nitrogen distance for the helical peptides (n = 3–5). (c) Dependence of
kapp on the number of intramolecular hydrogen bonds. (Data points
from top to bottom and left to right in (a) and (c) represent derivatives
with increasing number of Aib units).
Fig. 2 (a) Cyclic voltammograms of ferrocene-derivatised oligopeptide
(n = 5) modified SWCNTs/Si electrode in 0.1 mol Lꢀ1 TBAPF6/
CH3CN solution, with the scan rate v of 5, 10, 20, 50, 100, 200 and
500 mV sꢀ1 from the centre to upright. (b) Baseline subtracted cyclic
voltammogram at 200 mV sꢀ1
.
c
This journal is The Royal Society of Chemistry 2012
Chem. Commun., 2012, 48, 1132–1134 1133

diruthenium structure that also shows a slope transition and
hence two constants.13 We believe this difference to be attri-
butable to a combination of the donor, bridge and acceptor.1,36
The structures giving rise to the first three points in Fig. 3a
adopt a disordered conformation and hence lack defined intra-
molecular hydrogen bonding. Here the electron transfer rate
constant is clearly dependent on the number of Aib units and
hence the iron-to-terminal nitrogen distance. By comparison,
the three helical structures (represented by the last three points
in Fig. 3a) possess well-defined intramolecular hydrogen
bonding (1, 2, and 3 bonds respectively7,15) that defines their
secondary helical structure and hence the iron-to-terminal
nitrogen distance and mechanism of electron transfer. This
dependence of kapp on the number of intramolecular hydrogen
bonds is depicted in Fig. 3c. The electron transfer rate constant
depends strongly on intramolecular hydrogen bonding, which
facilitates the observed electron hopping mechanism. This is
consistent with theoretical studies,37 and experimental work that
reveals that an increase in the number of intramolecular hydrogen
bonds results in better donor/acceptor electronic coupling.
A previous study on oligopeptides reports a significant
decrease in kapp on increasing the number of intramolecular
hydrogen bonds from zero to one,7 with a much reduced
decrease for larger sequences containing further intramolecular
hydrogen bonding. The same phenomenon is observed in
Fig. 3c. However electron transfer was reported to occur via
an electron superexchange mechanism in the previous study.7
We suggest that these data are consistent with a transition from
superexchange to a hopping mechanism, due to a change from a
disordered to a well-defined helical conformation. Furthermore,
our results suggest a reinterpretation of the observed weak
dependence12 between the kapp and number of intramolecular
hydrogen bonds for helical oligopeptides in solution containing
p-cyanobenzamide donor and tertbutylperoxide acceptor
groups. Our work indicates an electron transfer hopping
mechanism with participation from the constituent intra-
molecular hydrogen bonds, rather than the previously reported
electron transfer superexchange mechanism.
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In conclusion, electrochemical studies are reported on oligomers
of Aib attached to a single-walled carbon nanotube array/p-silicon
(100) electrode to begin to unravel factors influencing the
mechanism of electron transfer. Our data suggests that electron
transfer in helical structures occurs by a hopping mechanism,
with the amide bonds providing hopping sites, and facilitation
from intramolecular hydrogen bonds. Shorter conformationally
disordered sequences undergo electron transfer via an alternative
electron superexchange mechanism. A mechanistic transition is
apparent on increasing the number of Aib units from 2 to 3.
The work was financially supported by the Australian
Research Council (DP0985176).
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Notes and references
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c
1134 Chem. Commun., 2012, 48, 1132–1134
This journal is The Royal Society of Chemistry 2012