S. oneidensis; and 6–61 mV for S. algae [121, 124, 125], in agreement with the
modest redox-linked structural modifications that occur in all three STCs. Furthermore, protonation has a considerable influence (redox–Bohr effect) on the redox
properties of the hemes (covering a range of −4 to −36 mV for S. frigidimarina
NCIMB400; −9 to −56 mV for S. oneidensis MR-1; and −1 to −51 mV for
S. algae DSM 9167 [121, 124, 125], with heme III having in all three STCs the
strongest redox-Bohr interaction, with a value similar to those reported for protonation of heme propionates [127]. In comparison, all three studied STC differ in
their relative order of oxidation of the hemes due to changes that have occurred over
time in their amino acid composition and/or structural arrangement. However, these
three STC still possess a common feature that is heme III always presenting the
highest reduction potential, and therefore is always the last heme to be oxidised
[121, 124, 125].
In vitro binding studies showed that STC could interact with both inner membrane cytochrome CymA and outer-membrane protein MtrA from the MtrCAB
complex [97]. These studies also showed that STC interacts with its redox partners,
CymA and MtrA, through a single heme (heme IV), which forces detachment from
the donor before attaching to the acceptor, preventing the formation of stable redox
complexes that can span the periplasmic space of Shewanella [97]. Interestingly,
although STC and FccA coexist and are highly abundant in the periplasmic space of
Shewanella, they do not exchange electrons among themselves. This ensures that
electron transport across the periplasmic space via these two proteins is segregated
[97].
4.3 Outer Membrane
In order to reduce insoluble electron acceptors, electrons must cross the outer
membrane and reach the cell exterior. Several redox proteins from Shewanella have
been shown to be associated or bound to the outer membrane. Of these, the
MtrCAB-OmcA protein complex is required to achieve maximal extracellular iron
reduction rates [31, 128–130]. The genes encoding for this complex are clustered in
an operon organized in the order: omcA-mtrC-mtrA-mtrB, where MtrC and OmcA
are decaheme cytochromes present at the cell surface, MtrA is a decaheme
periplasmic cytochrome and MtrB is a porin in which MtrA and MtrC are
embedded on [131, 132].
4.3.1 MtrB
The outer-membrane ß-barrel protein MtrB is a 78 kDa protein with no cofactors
but essential for EET [128]. Its pore size is estimated to be approximately
70 Â 55 Â 45 Å and embed MtrA and MtrC [132, 133]. The role of MtrB in metal
reduction was first demonstrated by showing that a MtrB knock-out mutant strain
lost its ability to reduce Fe(III) and Mn(IV) oxides [128]. MtrB knock-out mutants
in S. oneidensis MR-1 showed mis-localization of both outer-membrane cytochromes MtrC and OmcA [134]. Furthermore, it was also demonstrated that the
Bacterial Power: An Alternative Energy Source
227
modest redox-linked structural modifications that occur in all three STCs. Furthermore, protonation has a considerable influence (redox–Bohr effect) on the redox
properties of the hemes (covering a range of −4 to −36 mV for S. frigidimarina
NCIMB400; −9 to −56 mV for S. oneidensis MR-1; and −1 to −51 mV for
S. algae DSM 9167 [121, 124, 125], with heme III having in all three STCs the
strongest redox-Bohr interaction, with a value similar to those reported for protonation of heme propionates [127]. In comparison, all three studied STC differ in
their relative order of oxidation of the hemes due to changes that have occurred over
time in their amino acid composition and/or structural arrangement. However, these
three STC still possess a common feature that is heme III always presenting the
highest reduction potential, and therefore is always the last heme to be oxidised
[121, 124, 125].
In vitro binding studies showed that STC could interact with both inner membrane cytochrome CymA and outer-membrane protein MtrA from the MtrCAB
complex [97]. These studies also showed that STC interacts with its redox partners,
CymA and MtrA, through a single heme (heme IV), which forces detachment from
the donor before attaching to the acceptor, preventing the formation of stable redox
complexes that can span the periplasmic space of Shewanella [97]. Interestingly,
although STC and FccA coexist and are highly abundant in the periplasmic space of
Shewanella, they do not exchange electrons among themselves. This ensures that
electron transport across the periplasmic space via these two proteins is segregated
[97].
4.3 Outer Membrane
In order to reduce insoluble electron acceptors, electrons must cross the outer
membrane and reach the cell exterior. Several redox proteins from Shewanella have
been shown to be associated or bound to the outer membrane. Of these, the
MtrCAB-OmcA protein complex is required to achieve maximal extracellular iron
reduction rates [31, 128–130]. The genes encoding for this complex are clustered in
an operon organized in the order: omcA-mtrC-mtrA-mtrB, where MtrC and OmcA
are decaheme cytochromes present at the cell surface, MtrA is a decaheme
periplasmic cytochrome and MtrB is a porin in which MtrA and MtrC are
embedded on [131, 132].
4.3.1 MtrB
The outer-membrane ß-barrel protein MtrB is a 78 kDa protein with no cofactors
but essential for EET [128]. Its pore size is estimated to be approximately
70 Â 55 Â 45 Å and embed MtrA and MtrC [132, 133]. The role of MtrB in metal
reduction was first demonstrated by showing that a MtrB knock-out mutant strain
lost its ability to reduce Fe(III) and Mn(IV) oxides [128]. MtrB knock-out mutants
in S. oneidensis MR-1 showed mis-localization of both outer-membrane cytochromes MtrC and OmcA [134]. Furthermore, it was also demonstrated that the
Bacterial Power: An Alternative Energy Source
227