Geobacter's pili conduct
electrons along their length using the rings on aromatic amino acids, according
to a study in mBio this week. Contrary
to all other known forms of biological electron transport, in which electrons
are carried by discrete entities and passed from one to another, Geobacter's pili have a core of aromatic
amino acids that turn these hair-like appendages into functioning electron-carrying
biological wires, adding credence to a controversial idea in biology.
"It's the aromatic amino acids that make it a
wire," says lead author Derek Lovley. Lovley and his colleagues developed
a strain of Geobacter, Aro-5, that
lacked aromatic amino acids in parts of the pili implicated in electron
conduction, replacing them with smaller, non-aromatic amino acids. Without the
aromatic amino acids, Lovley says, the pili are nothing more than protein
strings. Importantly, Aro-5's pili were complete with OmcS, a multi-heme c-type
cytochrome essential for iron oxide reduction that was long suspected of
carrying the electrons along the length of the pili. But the presence of
working OmcS wasn't enough.
"We showed it's not good enough to just make the string
- you've got to make a wire," says Lovley.
Geobacter pili have metallic-like conductivity
G. sulfurreducens respires by removing
electrons from organic materials and funneling them to iron oxides or to other
microorganisms, much the way humans pull electrons out of organic molecules in
food and dump them on oxygen. The bacteria use their pili to reach out to iron
oxides or other microbes, transferring the "waste" electrons along
the structure to the destination. Geobacter's
pili are only 3-5 nanometers wide, but they can be 20 micrometers long, many
times longer than the cell itself.
Trafficking in electrons is how all living things breathe,
but it is normally carried out by discrete proteins or other molecules that act
like containers for shuttling electrons from one place to another. Lovley says
earlier results showed the pili in G.
sulfurreducens possess metallic-like
conductivity, the ability to carry electrons along a continuous structure, a
controversial finding.
To investigate how pili accomplish this singular feat,
Lovley says they looked to non-biological organic materials that can conduct
electricity. "In those synthetic materials, it's aromatic compounds that
are responsible for the conductivity. We hypothesized that maybe it's similar
in the Geobacter pili. In this case,
it would be aromatic amino acids." Aromatic compounds have a highly stable
ring-shaped structure made of carbon atoms.
Turning to the pili, Lovley says his group compared the Geobacter
pilus protein, PilA with those of other pili-makers, including Pseudomonas,
Neisseria and Vibrio species, that aren't capable of long-range
electron transport. By comparison, Geobacter
lacks a highly conserved N-terminal
domain these other sequences retain. Lovley's group guessed that the aromatic
amino acids in this area where Geobacter
is atypical could be carrying electrons via overlapping pi-pi orbitals.
Using genetic techniques, they developed a strain of Geobacter, Aro-5, that makes pili that
lack aromatic amino acids in this key region, then they tested whether these
pili could still conduct electricity. They could not. Removing the aromatic
amino acids was a bit like taking the copper out of a plastic-covered
electrical wire: no copper means no current, and all you're left with is a
string.
Removing aromatic amino acids from the pili prevents the
bacteria from reducing iron, too, says Lovley, an important point because it
adds further proof that Geobacter
uses its pili as nanowires for carrying electrons to support respiration.
Where to go from here?
Metal reducers like Geobacter
show a lot of promise for use in fuel cells, says Lovley, and by feeding
electrons to methanogens, they're an important component of anaerobic digesters
that produce methane gas from waste products. Understanding how they shuttle
their electrons around and how to optimize the way the pili function could lead
to better technologies.
Moving forward, Lovley says his own lab plans to explore the
possibilities of biological nanowires, exploring how to make them more or less
conductive. "The fact that we were able to make the physical filament, but
it's no longer a wire gives us a lot of power for looking at those
phenotypes," says Lovley.