Some microorganisms can establish a thick multilayer electrochemically active
biofilm, and through long-range conductive filamentous appendages, such as
nanowires or pili, achieve higher electron transfer rates and densities per surface
area when compared to cell monolayers [35]. Scanning tunneling microscopy
images show thin filaments with about 8 nm in diameter and 10 µm in length [35].
These conductive filamentous appendages allow the bacteria to conduct electrons
over a large distance within the multiple layers of a biofilm. In terms of morphology, Shewanella nanowires are partially composed of c-type cytochromes [28,
36–39]. This was demonstrated by deleting the genes coding for the
outer-membrane cytochromes, MtrC and OmcA, resulting in non-conductive
nanowires [38]. Also, deleting the gspG gene which is involved in the type II
secretion pathway, that is required for the proper export of the outer-membrane
cytochromes MtrC and OmcA to the cell exterior [40, 41], resulted in
non-conductive nanowires. Later studies using fluorescence microscopy revealed
that Shewanella nanowires are, in fact, extensions of the outer-membrane and
periplasm [42].
Other examples of conductive filaments are the pili [43] and the more recent
multiheme cytochrome OmcS filaments [44, 45] from the Geobacter genus. The
hypothesis that the pili might function as conductive filamentous appendages
resulted from the observation that pili were specifically expressed during growth on
insoluble electron acceptors [46]. Studies showed that type IV pilus monomer PilA
deletion mutant of G. sulfurreducens could not reduce Fe(III) oxide and displayed a
much lower current production in MFCs [28, 47]. The NMR structure of the PilA
monomer of G. sulfurreducens shows that it is shorter than the PilA from other
microorganisms [48]. Indeed, the truncation of PilA in G. sulfurreducens was
proposed to be essential for iron respiration, suggesting that an adaptive evolution
of this organism to dissimilatory iron reduction in natural environments has been
achieved with the truncation of this protein [49]. Using cryo-electron microscopy,
the structure of a different conductive filament was solved, with particle reconstructions showing that only the outer surface MHC OmcS monomers alone could
produce a perfect fit [44, 45]. This argues for conductive filaments in Geobacter to
be composed entirely of OmcS and that no arrangement with PilA monomers is
present, as previously proposed [50]. These observations provide a context for the
fact that, whereas the mechanism by which electrons are transferred along the PilA
filaments is still fiercely debated [51], the OmcS polymer provides a continuous
chain of hemes at close distance for efficient conduction along the length of the
whole filament [44].
2.2 Mediated EET
Besides direct EET, some bacteria can also reduce extracellular substrates through
mediated electron transfer, using small organic electron shuttles. These serve as the
terminal electron acceptors, and once reduced, can themselves transfer electrons to
iron oxides or anodes in MFCs.
Bacterial Power: An Alternative Energy Source
219
biofilm, and through long-range conductive filamentous appendages, such as
nanowires or pili, achieve higher electron transfer rates and densities per surface
area when compared to cell monolayers [35]. Scanning tunneling microscopy
images show thin filaments with about 8 nm in diameter and 10 µm in length [35].
These conductive filamentous appendages allow the bacteria to conduct electrons
over a large distance within the multiple layers of a biofilm. In terms of morphology, Shewanella nanowires are partially composed of c-type cytochromes [28,
36–39]. This was demonstrated by deleting the genes coding for the
outer-membrane cytochromes, MtrC and OmcA, resulting in non-conductive
nanowires [38]. Also, deleting the gspG gene which is involved in the type II
secretion pathway, that is required for the proper export of the outer-membrane
cytochromes MtrC and OmcA to the cell exterior [40, 41], resulted in
non-conductive nanowires. Later studies using fluorescence microscopy revealed
that Shewanella nanowires are, in fact, extensions of the outer-membrane and
periplasm [42].
Other examples of conductive filaments are the pili [43] and the more recent
multiheme cytochrome OmcS filaments [44, 45] from the Geobacter genus. The
hypothesis that the pili might function as conductive filamentous appendages
resulted from the observation that pili were specifically expressed during growth on
insoluble electron acceptors [46]. Studies showed that type IV pilus monomer PilA
deletion mutant of G. sulfurreducens could not reduce Fe(III) oxide and displayed a
much lower current production in MFCs [28, 47]. The NMR structure of the PilA
monomer of G. sulfurreducens shows that it is shorter than the PilA from other
microorganisms [48]. Indeed, the truncation of PilA in G. sulfurreducens was
proposed to be essential for iron respiration, suggesting that an adaptive evolution
of this organism to dissimilatory iron reduction in natural environments has been
achieved with the truncation of this protein [49]. Using cryo-electron microscopy,
the structure of a different conductive filament was solved, with particle reconstructions showing that only the outer surface MHC OmcS monomers alone could
produce a perfect fit [44, 45]. This argues for conductive filaments in Geobacter to
be composed entirely of OmcS and that no arrangement with PilA monomers is
present, as previously proposed [50]. These observations provide a context for the
fact that, whereas the mechanism by which electrons are transferred along the PilA
filaments is still fiercely debated [51], the OmcS polymer provides a continuous
chain of hemes at close distance for efficient conduction along the length of the
whole filament [44].
2.2 Mediated EET
Besides direct EET, some bacteria can also reduce extracellular substrates through
mediated electron transfer, using small organic electron shuttles. These serve as the
terminal electron acceptors, and once reduced, can themselves transfer electrons to
iron oxides or anodes in MFCs.
Bacterial Power: An Alternative Energy Source
219