in Biology | DNA Electron Transport Dynamics |
Electron Transport Dynamics*
Charge transfer in supramolecular assemblies of DNA is unique
because of the notion that the π-stacked bases within the
duplex may mediate the transport, possibly leading to damage and/or
repair. The phenomenon of transport through π-stacked arrays
over a long distance has an analogy to conduction in molecular
electronics, but the mechanism still needs to be determined. To
decipher the elementary steps and the mechanism, one has to directly
measure the dynamics in real time and in suitably designed, structurally
well-characterized DNA assemblies. Since the first report on conductive
one-dimensional DNA crystals more than 30 years ago, different
methods have been used for the study of conductivity, the latest
of which is the measurement of conductance on the mesoscopic scale,
which suggests a large band-gap semiconductor behavior. Charge
transfer by photoinduced reactions between donors and acceptors
has provided a useful methodology for exploring the mechanism
in DNA; the donor and acceptor were either noncovalently or covalently
bound to DNA. Evidence for long-range oxidative damage was also
demonstrated. However, results for different systems have shown
different values for the distance range over which the transfer
is efficient, in part because of measurements of the yield in
Although many studies have focused on systems with a tethered
hole donor, a careful study of the effects of stacking and distance
on charge transfer requires DNA assemblies unperturbed by donor/acceptor
probes. At LMS, we study DNA assemblies with the donor and acceptor
being nucleic acid bases. These systems are unique because (i)
there are only minor structural perturbations arising; (ii) no
ambiguities occur with respect to distance separating donors and
acceptors; (iii) the assemblies are structurally well defined
and well characterized; and (iv) much is known about the steady-state
quenching of fluorescence.
role of dynamic base motions in DNA ET is not fully understood,
as it involves a range of timescales and different motions. At
LMS, our approach has been to measure the femtosecond dynamics
of charge transport processes occurring between bases within duplex
DNA. By monitoring the population of an initially excited 2-aminopurine,
an isomer of adenine, we can follow the charge transfer process
and measure its rate. We then study the effect of different bases
next to the donor (acceptor), the base sequence, and the distance
dependence between the donor and acceptor. We find that the charge
injection to a nearest neighbor base is crucial and the time scale
is vastly different: 10 ps for guanine and up to 512 ps for inosine.
Depending on the base sequence the transfer can be slowed down
or inhibited, and the distance dependence is dramatic over the
range of 14 Å. These observations provide the time scale,
and the range and efficiency of the transfer.
time scales show the distinct local and base-mediated dynamics
over three bridge bases, and the dependence on the nature of the
bases involved. Based on the facts that the rates are on the picosecond
time scale, the base-mediated (superexchange-type) process significantly
slows down with distance (≈14 Å), the overall rate
is controlled by the initial charge injection (even if the transfer
between bases is faster), and the efficiency decreases for each
step because of dynamical disorder, we conclude that DNA does
not exhibit an efficient molecular wire behavior. Long-range transport
must occur on a longer time scale and with a different mechanism,
possibly by hopping migration.
To further explore the effects of base dynamics, we have examined
ET between DNA bases directly as a function of temperature through
femtosecond transient absorption spectroscopy. Our investigations
employ photoexcited 2-aminopurine (Ap*) as a dual reporter of
DNA base dynamics and DNA-mediated ET. Ap undergoes normal Watson-Crick
pairing with T and is well stacked. ET reactions between Ap* and
nucleotides, as well as Ap* and bases in DNA have been extensively
characterized. In DNA, ET between Ap* and G can be distinguished
from other modes of quenching by comparing redox-active G-containing
duplexes to otherwise identical duplexes in which the G is replaced
by inosine (I), an analogue of G that is essentially inactive
towards ET with Ap*.
results show that ultrafast DNA dynamics play a defining role
in DNA-mediated ET. This role originates from the fact that base
motions occur on the ET timescale. As ET occurs only through DNA
assemblies that have a specific, well-coupled alignment of the
DNA bases, motions of the DNA bases that lead to these ET-active
conformations can serve as a gate for ET reactions, and thus modulate
the rate constants and yields of ET.
results provide compelling experimental evidence that DNA ET cannot
be approximated by models designed for more static donor-acceptor
assemblies. Fluctuations of DNA bases must be a part of the descriptions
of ET dynamics, especially because conformational gating necessarily
becomes more important as the DNA bridge is lengthened.
*The text above has been adapted from the following publications.
Ultrafast Unequilibrated Charge Transfer: A New Channel
in the Quenching of Fluorescent Biological Probes,
C. Wan, T. Xia, H.-C. Becker, A. H. Zewail, Chem. Phys. Lett.
2005, 412, 158.
Ultrafast Dynamics in DNA-Mediated Electron Transfer: Base
Gating and the Role of Temperature, M. A. O'Neill, H.-C. Becker,
C. Wan, J. K. Barton, A. H. Zewail, Angew. Chem., Int. Ed. 2003,
Femtosecond Charge Transfer Dynamics of a Modified DNA Base:
2-Aminopurine in Complexes with Nucleotides, T. Fiebig,
C. Wan, A. H. Zewail, Chem. Phys. Chem. 2002, 3, 781.
Femtosecond Direct Observation of Charge Transfer between Bases
in DNA, C. Wan, T. Fiebig, O. Schiemann, J. K. Barton, A. H.
Zewail, Proc. Natl. Acad. Sci. USA 2000, 97, 14052.