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Bio-batteries: creating energy from bacteria

As renewable energy begins to gain traction as a serious possibility for society's future needs, we explore a truly renewable source: bacteria.

The potato-powered clock is a nostalgic flashback from the childhood biology lessons of most of us, but a small group of scientists believe generating electricity from bacterial organisms could become a viable option.

New insights into the mechanics of a novel aspect of bacterial respiration could help speed the development of microbial power plants capable of generating electricity from industrial wastewater or sea-floor sediments, and bacterial factories that manufacture high-value chemicals and fuels using just solar power and carbon dioxide.

Recent research reported by Dr Tom Clarke's team at the University of East Anglia's Department of Biological Sciences has shown how thousands of tiny molecular wires embedded in the surface of a bacterium called Shewanella oneidensis can directly transmit an electric current to inorganic minerals such as iron and manganese oxides, or the surface of electrodes. The phenomenon, known as direct extracellular electron transfer (DEET), occurs because of the way that some bacteria living in environments lacking oxygen export electrons that are generated through their respiratory cycle. Examples include Shewanella, and some species of another bacterium known as Geobacter.

Cellular respiration occurs in all living organisms, and involves a cyclical series of chemical reactions that take place within a body's cells to convert biochemical energy taken in as food or nutrients into a source of energy that cells can tap into to power all the biochemical processes they carry out.

This process generates excess electrons that, in most organisms, are passed to oxygen (generating water as a byproduct) or, in the case of microbes living an oxygen-free environment such as mud sediments, the electrons are passed to other mineral ions taken in by the cell. What scientists have found over recent years, however, is that a range of microorganisms have developed ways of directly exporting the excess electrons from the cell. They do this by shuttling the electrons along tiny molecular wires that protrude about 2.5nm from the cell surface.

Microbial fuel cell

Grow these bacteria on an electrode and you effectively end up with the anode half of a battery. Couple this anode to a cathode, feed the bacteria with carbon-based organic matter, say, from industrial wastewater, and you can construct a microbial fuel cell, or MFC, that generates electricity, albeit in small amounts.

Shewanella oneidensis, a bacterium that thrives in environments contaminated by heavy metals, is one of the organisms that displays this electron-shuttling capability, and the work by Clarke's group at the UEA, collaborating with a team at the US Department of Energy's (DoE) Pacific Northwest National Laboratory, has shown how Shewanella's molecular wires can transport electrons out of the cell to a suitable surface on which the bacterium is growing.

"The results from our experiments were striking," Dr Clarke claims. "These bacterial wires are effectively just like the wiring in a house. A current flowed backwards and forwards incredibly quickly, and much faster than is needed for respiration."

Harnessing Shewanella as a source of electricity at a scale suitable for ploughing electricity back into a national grid system probably isn't going to be feasible, simply because the organisms don't generate enough current, Dr Clarke continues. However, their ability to give electrons to metals and minerals can be exploited for bioremedial applications, such as the reduction of soluble heavy metals present in soil into insoluble forms that can't leach into the groundwater. This is one of the avenues of research that the Pacific Northwest Laboratory researchers are pursuing.

But what's even more exciting, he claims, is the potential to exploit the reverse process: putting electrons back into bacteria such as Shewanella through the wires, and genetically engineering the microorganisms to make useful compounds, including fuels and polymer precursors, directly from carbon dioxide.

Known as microbial electrosynthesis, this'is basically an artificial photosynthesis, which is how plants generate sugars from sunlight, CO2 and water. But rather than sunlight itself, the bacteria will accept electrons as a power source, which they use to produce carbon-based compounds from CO2.

It's already feasible commercially to 'farm' photosynthetic algae as a means of producing compounds that can be converted into fuels or other products. However, as Clarke points out, this approach swallows up large areas of land, and is associated with environmental degradation. In contrast, microbial electrosynthesis could feasibly be exploited anywhere there is sunlight, by using photovoltaic panels to power the bacteria, and a source of water and CO2 gas, (industrial waste gas will do nicely) to feed the bacteria so they can manufacture carbon-based products.

Electrosynthesis as a technology is also distinct from the use of other bacteria such as Escherichia coli, and yeast fermentation, for manufacturing chemical compounds. "Genetically engineered bacteria and yeast are used widely in commercial settings to manufacture proteins and other compounds, intermediates and even drugs, but they don't photosynthesise, so you have to fuel them with a sugar of some sort, which adds significant cost to the process," Clarke explains. "In contrast, electricity is cheap, and CO2 is a waste product of many industrial processes and fossil-fuel burning. If we can power up bacteria such as Shewanella with electrons, for example by placing them on electrodes connected to solar panels, and give them CO2 as a source of carbon, we could feasibly use this artificial photosynthetic process to generate high-value products."

An environmental win-win situation

Harnessing the ability of Shewanella and other microorganisms to pass electrons to and from electrodes (and thus the devices they are connected to) is a field known as electromicrobiology. "From an environmental perspective it's a win-win situation," says Professor Korneel Rabaey, at the University of Ghent's Department of Biochemical and Microbial Technology.

Previously a founder of the Centre for Microbial Electrosynthesis at the University of Queensland, Professor Rabaey was instrumental in the implementation of a pilot-scale microbial bioelectrochemical system (BES) plant at a Foster's brewery in Yatala, Queensland, five years ago. This pilot plant used bacteria to generate electrical power from the brewery's own wastewater, and produce caustic soda, which the brewery needs in large amounts to clean its tanks. A similar pilot project has since been established at a paper manufacturing plant, to generate the hydrogen peroxide required in the production process.

The University of Queensland's work has in addition led to the creation of a spin-out firm, Bilexys, which is developing bioelectrochemical systems that couple wastewater treatment with commercial-scale production of chemicals. "These pilot plants demonstrate that the concept will work in the real world, and could provide industry with options for generating chemicals required on site, with very little energy input, and the added benefit of cleaning up their waste at the same time," Prof Rabaey comments. "As more of these pilot plants come on stream the technology will be seen as commercially viable and spur further development of new processes."

Biofactories powered by electrons

It's important to distinguish between the generalised concept of using bacteria to clean up wastewater, and the use of bioelectrochemical synthesis by organisms such as Shewanella, Prof Rabaey stresses. "The treatment of wastewater using anaerobic bacteria to break down the organic content is well-recognised, and applied widely to produce methane-rich biogas." In fact, there are upwards of 3,000 plants in Europe alone that produce biogas in this way, using a mix of bacteria that can break down complex carbon compounds into ever-smaller components, he points out.

"What we can't yet do is manufacture clean, high-value chemicals from wastewater, and this is where bioelectrochemical synthesis by bacteria such as Shewanella could revolutionise the production of fuels, biopolymers and other substances from wastewater, using just cheap sources of electricity. The bacteria can already make some small molecules, but we hope to genetically engineer the microorganisms so that they produce more complex molecules, in much the same way that we can now engineer yeast and the bacterium E. coli as biofactories. However, with bioelectrochemical synthesis we don't need to plug sugars into the organisms as building blocks for them to manufacture the final product."

Work toward this goal is still in relative infancy, however. "On the one hand we have bacteria such as Shewanella that can carry out artificial photosynthesis using cheap electricity, but that can currently only manufacture a limited range of useful compounds," says Prof Rabaey. "On the other hand we have an arsenal of microorganisms – like E. coli and yeast – that have the biological machinery necessary to produce a large number of useful compounds, and which can be engineered relatively easily, but which don't display the electron-shuttling machinery required for them to be fuelled with electricity."

Work to develop the technologies that will allow scientists to modify electron-accepting species of bacteria including Shewanella, Geobacter, and species of the bacterium Clostridium, is being pioneered by Professor Derek Lovley at the University of Massachusetts (UMass) at Amherst, who discovered the first species of Geobacter, known as Geobacter metallireducens, in sand sediment in the Potomac river in 1987.

Bacterial conductivity

Professor Lovley spearheads the Geobacter project (www.geobacter.org) at UMass, which is investigating both the electricity generating – i.e. microbial fuel cell – and electrobiosynthetic capabilities of the bacterium. Geobacter excels at generating electricity, but Prof Lovley's thinking mirrors that of Clarke and Rabaey, in that he believes it's unlikely we'll see the development of Geobacter- or Shewanella-based wastewater treatment plants that generate large amounts of electricity as a byproduct. "Our work on microbial fuel cells relates in the main to US Office of Naval Research-funded projects that are looking at harvesting electricity from the mud at the bottom of the ocean to run monitoring devices, which require only a little power."

One potential application of the electricity-generating capacity of Geobacter could be the development of bioelectric sensors for organic compounds, Prof Lovley suggests. "In this type of sensor the bacteria would be coupled to an electrode, and a positive result would be registered as a small electric current." It's a case of thinking how to exploit the electricity-generating capabilities of relevant organisms at the smaller, rather than larger scale. "Applications where you don't need to generate a lot of power represent good opportunities for microbial fuel cells and organisms that can carry out DEET."

The bioremediation applications are, in contrast, manifold, Prof Lovley stresses. One of the UMass projects, in collaboration with oil companies, aims to harness Geobacter's ability to oxidise organic matter as a means of removing hydrocarbon contaminants from soil and ground water. Work by the UMass teams is separately attempting to map the genetic code of different Geobacter species, and this should help predict how the bacteria will behave under different environmental conditions, and allow scientists to determine the best strains of the organism activities such as cleaning up specific contaminants.

UMass research on the process of electrosynthesis (putting electrons back into the bacteria) is centred on other microorganisms, such as species of Clostridium, which appear much better suited than Geobacter to applications in which the organisms are fuelled with electrons to generate products from carbon dioxide, Prof Lovley adds. "Geobacter is the better of the two organisms for generating electricity, whereas Clostridium is well suited to electrosynthetic applications."

What the researchers don't yet know, however, is how Clostridium gets its electrons in and out of the cell. The organism doesn't produce molecular wires like Shewanella and Geobacter. "Clostridium appears to have a totally different outside chemistry to Shewanella, and uncovering how it works is something we hope to achieve over the coming years".

Optimising bioproduction

One of the UMass team's big technological breakthroughs came last year, with the development of a bioengineering platform that will allow scientists to genetically modify the Clostridium species so that the microorganism will use the CO2 and electrical energy to produce very simple organic compounds and convert them into more complicated hydrocarbons. "It's the same basic idea as manipulating other bacteria, in that you can take some genes out and put others in, to direct the cell to manufacture the compound you want, or make a precursor or building block that can easily be modified into the final product."

Moreover, further insights into the structure of nanofilaments produced by species such as Geobacter and Shewanella could pave the way to the development of microcircuitry based on biological wiring as a completely new approach to interfacing biology with electronics. For example, Prof Lovley suggests, Geobacter has been found to exhibit transistor properties, and can function as supercapacitors for electron storage.

"This lends itself to the potential to grow microbial electronic components from inexpensive feedstocks, for mass production. The microbial wires are extraordinarily durable for a biological protein, and bioelectronics have the added advantage of being functional in water." However, he stresses, the practical applications of such technologies are still at the conceptual stage.

So, do these mud-and soil-dwelling microorganisms represent a promise of cheap energy for all? It seems unlikely that DEET will realistically quench the world's thirst for electricity, although the ability of these bacteria to generate an electric current may prove useful for developing microbial fuel cell-based biosensors and small-scale biobatteries. What's far more likely is that Geobacter, Clostridium and Shewanella will have much more widespread and commercially viable applications in fields such as bioremediation and wastewater cleanup, and the synthesis of valuable industrial compounds, intermediates, and fuels.

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