becomes spontaneous when the menaquinol/menaquinone balance is shifted
towards menaquinol. Once the electrons enter the heme network, electron flow to
the metal oxides becomes thermodynamically favorable due to progressively less
negative redox potentials of the electron transfer proteins that are downstream of
CymA [101].
Despite the importance of CymA for EET, the quinol dehydrogenase complex
SirCD is capable of partially replacing it, restoring the capability of Shewanella
DcymA strains to use Fe(III), fumarate or DMSO as terminal electrons acceptors
[102]. Shewanella contains another tetraheme cytochrome attached to the
inner-membrane denominated TorC [103]. Like CymA, TorC is a quinol dehydrogenase and is involved in the reduction of the terminal electron acceptor,
Trimethylamine N-oxide (TMAO) to trimethylamine (TMA). This capability is the
origin of the designation putrefaciens for the smell of rotten fish [104].
4.2 Periplasmic Space
In S. oneidensis MR-1, the periplasmic space has a width of approximately 235 Å
[105] and contains an abundance of soluble electron transfer proteins (e.g. MHCs),
in extremely high concentration, estimated to reach the mM range [106]. These
proteins can be terminal reductases of soluble electron acceptors, or proteins that
mediate electron transfer to the outer-membrane proteins for the reduction of
insoluble electron acceptors. The two most abundant periplasmic cytochromes are
the tetraheme flavocytochrome c FccA [97, 107, 108] and the small tetraheme
cytochrome c STC [97, 107, 109].
4.2.1 FccA
FccA, a 64 kDa tetraheme c-type flavocytochrome, is a unidirectional fumarate
reductase with a FAD cofactor in the active site [110]. This enzyme is unique in
comparison to other fumarate reductases since it is a monomeric and soluble
periplasmic protein. X-ray crystal structures of FccA from S. frigidimarina
NCIMB400 and S. oneidensis MR-1 are available [111, 112], showing that these
proteins fold into three domains: a N-terminal cytochrome domain with four bis–
histidine low-spin c-type hemes, a C-terminal flavoprotein domain with a
non-covalently bound FAD group and a clamp domain that was proposed to control
the access to the active site of the enzyme. The hemes found in the N-terminal
domain of FccA are arranged in a quasi-linear architecture that allows an efficient
conduction of the electrons across the length of the protein to the FAD catalytic
center [111–113]. Electron transfer to the active site is performed by heme IV,
which is in close proximity (%5 Å) to the FAD cofactor.
A microscopic redox characterization was obtained for FccA from S. frigidimarina NCIMB400 and S. oneidensis MR-1, revealing that despite their similar
structure the details of the redox properties of the hemes are different [113, 114].
However, the differences are compatible with a common theme of internal control
of the electron transfer flow that appears to direct electrons to the flavin catalytic
Bacterial Power: An Alternative Energy Source
225
towards menaquinol. Once the electrons enter the heme network, electron flow to
the metal oxides becomes thermodynamically favorable due to progressively less
negative redox potentials of the electron transfer proteins that are downstream of
CymA [101].
Despite the importance of CymA for EET, the quinol dehydrogenase complex
SirCD is capable of partially replacing it, restoring the capability of Shewanella
DcymA strains to use Fe(III), fumarate or DMSO as terminal electrons acceptors
[102]. Shewanella contains another tetraheme cytochrome attached to the
inner-membrane denominated TorC [103]. Like CymA, TorC is a quinol dehydrogenase and is involved in the reduction of the terminal electron acceptor,
Trimethylamine N-oxide (TMAO) to trimethylamine (TMA). This capability is the
origin of the designation putrefaciens for the smell of rotten fish [104].
4.2 Periplasmic Space
In S. oneidensis MR-1, the periplasmic space has a width of approximately 235 Å
[105] and contains an abundance of soluble electron transfer proteins (e.g. MHCs),
in extremely high concentration, estimated to reach the mM range [106]. These
proteins can be terminal reductases of soluble electron acceptors, or proteins that
mediate electron transfer to the outer-membrane proteins for the reduction of
insoluble electron acceptors. The two most abundant periplasmic cytochromes are
the tetraheme flavocytochrome c FccA [97, 107, 108] and the small tetraheme
cytochrome c STC [97, 107, 109].
4.2.1 FccA
FccA, a 64 kDa tetraheme c-type flavocytochrome, is a unidirectional fumarate
reductase with a FAD cofactor in the active site [110]. This enzyme is unique in
comparison to other fumarate reductases since it is a monomeric and soluble
periplasmic protein. X-ray crystal structures of FccA from S. frigidimarina
NCIMB400 and S. oneidensis MR-1 are available [111, 112], showing that these
proteins fold into three domains: a N-terminal cytochrome domain with four bis–
histidine low-spin c-type hemes, a C-terminal flavoprotein domain with a
non-covalently bound FAD group and a clamp domain that was proposed to control
the access to the active site of the enzyme. The hemes found in the N-terminal
domain of FccA are arranged in a quasi-linear architecture that allows an efficient
conduction of the electrons across the length of the protein to the FAD catalytic
center [111–113]. Electron transfer to the active site is performed by heme IV,
which is in close proximity (%5 Å) to the FAD cofactor.
A microscopic redox characterization was obtained for FccA from S. frigidimarina NCIMB400 and S. oneidensis MR-1, revealing that despite their similar
structure the details of the redox properties of the hemes are different [113, 114].
However, the differences are compatible with a common theme of internal control
of the electron transfer flow that appears to direct electrons to the flavin catalytic
Bacterial Power: An Alternative Energy Source
225