Microbe power: electron-transfer protein structure

Electrifying microbes

X-ray diffraction has been used to reveal the structure of proteins attached to the surface of the microbe Shewanella oneidensis, a species found in deep-sea anaerobic habitats. These proteins can transfer electrons making this micro-organism potentially rather interesting as an electricity-generating system. The research could allow researchers to "tether" bacteria directly to electrodes creating efficient microbial fuel cells or bio-batteries powered by human or animal waste. Such an advance could also hasten the development of system based on microbial agents that can clean up oil spills or provide a new approach to remediating radioactive waste.

"This is an exciting advance in our understanding of how some bacterial species move electrons from the inside to the outside of a cell," explains UEA's Tom Clarke. "Identifying the precise molecular structure of the key proteins involved in this process is a crucial step towards tapping into microbes as a viable future source of electricity."

In 2009, Tom Clarke, David Richardson and Julea Butt of the University of East Anglia together with colleagues Marcus Edwards, Andrew Gates, Andrea Hall, Gaye White, Justin Bradley, Nicholas Watmough and David Richardson in Norwich, UK and colleagues at the Pacific Northwest National Laboratory in Richlane, Washington, USA, Catherine Reardon, Liang Shi, Alexander Beliaev, Matthew Marshall, Zheming Wang, James Fredrickson, and John Zachara, demonstrated how bacteria can survive in oxygen-free environments. The microbes construct electrical wires that extend through their cell wall and make contact with a mineral to enable iron(III) oxide or manganese(IV) oxide respiration. The metals act as electron respiratory electron acceptors.

Heavy metal reduction

In the proteobacterium, Shewanella oneidensis, well known for its ability to reduce heavy metals and investigated for bioremediation, the process of iron respiration uses decaheme cytochromes. These proteins are present on the surface of the bacterial cell wall anchored at the termini of trans-outer-membrane electron transfer conduits. According to Clarke and colleagues writing in a new paper in PNAS, these cell-surface cytochromes might play various roles in mediating electron transfer directly to insoluble electron sinks, catalysing electron exchange with flavin electron shuttles and participating in extracellular intercytochrome electron exchange along what the team refers to as "nanowire appendages".

The researchers have now obtained an X-ray crystal structure at a "modest" 3.2 angstrom resolution of one example of these decaheme cytochromes known as MtrF. The structure has allowed the researchers to visualise for the first time the arrangement of the ten iron-centred heme groups in this protein. "The hemes are organized across four domains in a unique crossed conformation, in which a staggered 65-angstrom octaheme chain transects the length of the protein and is bisected by a planar 45-angstrom tetraheme chain that connects two extended Greek key split beta-barrel domains," the team explains.

This detailed structural revelation offers a new insight at the molecular level as to how the microbes can apparently carry out two seemingly unrelated reduction processes in the same system in tandem. These are the reduction of insoluble mineral substrates, the reduction of soluble substrates, such as flavins. The structure hints out how it is possible for cytochrome redox partners to exist in tandem at different termini of a trifurcated electron-transport chain on the cell surface, the team explains.

Interrogating validity

"Further biophysical work is now required to interrogate the validity of these mechanistic models, but this first structure of a member of the extracellular decaheme cytochrome family opens up many previously undescribed experimental lines with which to move the understanding of electron transfer at the microbe-mineral interface forward," the team says.

"We are some way away from the fuel cells but I think that these 'wires' may give us the opportunity to do some interesting things in the future," Clarke revealed to SpectroscopyNOW. "The ability to conduct a charge into a living cell could have some very interesting potential uses."

The views represented in this article are solely those of the author and do not necessarily represent those of John Wiley and Sons, Ltd.