The culprit is a class of microbial power plants capable of transferring electrons from inside their membranes to the outside world. By stripping electrons from organic “food” such as acetate or lactic acid and passing them to metallic compounds beyond their cell walls, these bacteria effectively “breathe” metals like humans and E. coli breathe oxygen.
Researchers studying “electromicrobiology” tend to focus on two genera, Geobacter and Shewanella. Derek Lovley at the University of Massachusetts, Amherst, isolated the former from Potomac River sediment in 1988 while looking for microorganisms that could “use iron the way we use oxygen.” He found that Geobacter has a gift for bioremediation of organic pollutants and heavy metals. It also has the ability to reduce iron oxides in the environment.
Years later, Lovley was approached by the US Office of Naval Research to figure out how electrodes placed in marine sediment generate power—a phenomenon the Navy was exploring to drive undersea instrumentation. Hypothesizing that Geobacter or related organisms could explain the phenomenon, Lovley gave the project to his then-postdoc, Daniel Bond, who is now an associate professor at the University of Minnesota, St. Paul.
Bond, who as a child enjoyed tinkering with electronic circuits, discovered that in the absence of oxygen an electrode immersed in marine sediment would acquire a bacterial coating, consisting mostly of members of the family Geobacteraceae. These bacteria could actually extract electrons from acetate or benzoate and pass them directly to the electrode—no chemical intermediates required—producing a measurable current. But, kill the culture, and the current dies too. (1)
Kenneth Nealson, now at the University of Southern California, stumbled across Shewanella oneidensis MR-1 (then known as Alteromonas putrefaciens MR-1) in 1988 while trying to explain high rates of manganese reduction in a freshwater lake in upstate New York. (2) S. oneidensis MR-1 was just one of 20 microbes he isolated that were able to convert manganese solids into soluble mineral. He focused on this organism purely for “experimental convenience,” since the microbe could grow in the presence of oxygen.
Shortly thereafter, a colleague in Korea named Hong Kim suggested that if S. oneidensis MR-1 could transfer electrons outside its cell walls, perhaps it could also function in what essentially is a microbial battery—that is, to do electrical work.
“How the heck do bacteria do this?” Nealson said. “How do they move electrons across a membrane that was designed specifically so that electrons couldn’t go across it?” It’s taken him and his colleagues nearly a quarter-century of research to answer that question.
A Beautiful Little Complex
Most well studied microbes, and eukaryotes for that matter, use membrane-bound electron transport chains to convert sugar into usable chemical energy. Electrons harvested from food pass back and forth across the membrane on chemical carrier molecules. As they do so, protons are pumped across the membrane, creating a charge gradient that drives ATP generation. Electrical microbes use the same basic processes, Lovley explained, except, “The very final step, where in a typical microbe or a eukaryote the electrons would go onto oxygen inside the cell, their final step is a route to get electrons outside the cell.”
In S. oneidensis MR-1, at least, that route involves a heme-rich protein complex that creates what is essentially a wire through the outer membrane. “You end up with a conduit that’s a continuous chain of 15 or 20 individual hemes,” Bond said. “It’s a beautiful little complex.”
Geobacter has a similar structure, although it evolved independently. And it can transfer those electrons directly to external molecules via conductive filamentous structures called pili, which function like “organic conducting polymers,” according to Lovley. In one recent study, his team used electrostatic force microscopy, a form of atomic force microscopy, to inject current into the pili and watch it propagate. The findings demonstrate that the pili function not by electrons hopping from carrier to carrier, as is common in biology, but like a traditional wire or carbon nanotube. “I wouldn’t have expected that,” he said. “This protein really functions in the same way.” (3)
Other bugs, like Shewanella, use ringed organic compounds, such as flavin mononucleotide, as electron shuttles to transfer its outbound electrons or use surface-bound cytochromes instead.
Geobacter and Shewanella are just the tip of the proverbial iceberg when it comes to electromicrobiology. All that’s required, it seems, is to stick an electrode in the ground, wait a few weeks, scrape off the resulting biofilm, and start isolating cells. “It’s like putting a sugar cube someplace and asking which kids are going to like it,” Nealson explained.
Each bug, of course, has unique properties. Just as some people are taller or faster than others, some microbes prefer one food to another, grow at different rates, or produce more or less electrons. “Depending on where the bacteria were and what they were doing before you isolated them… there will be a range of activities,” said Nealson.
Some can even run the electrical process in reverse. Bond’s lab has identified a microbe called Mariprofundus that can take up electrons from an electrode and pass them to oxygen—no actual food required at all. “They build all the biomass and do all their metabolism using nothing but a string of electrons,” he said.
Even Shewanella, as it turns out, has this activity, meaning the bacteria can grow on both sides of a microbial fuel cell, generating electrons at the anode and consuming them at the cathode. In such a configuration, Nealson said, Shewanella is “…completely schizophrenic. On the anode side it’s doing anaerobic metabolism, on the cathode side it’s doing aerobic metabolism. And you just hook them up with a wire. So you split the metabolic personality of this bug into two completely different sides of the fuel cell.”
Researchers have even found that microbes can transfer electrons to other species. Lovley reported earlier this year that Geobacter metallireducens can power methane generation by Methanosaeta harundinaceaby direct pili-mediated electron transfer, essentially coupling ethanol metabolism in the former with carbon dioxide reduction in the latter. (4)
Powering New Applications
Electrically active bacteria promise the ability to do work without exogenous energy. “This actually provides a whole new technology platform for engineers,” said Zhiyong “Jason” Ren, associate professor at the University of Colorado, Boulder.
Ren studies wastewater treatment, a traditionally power-hungry operation. “We actually currently use about 100 billion kilowatt-hours of electricity every year to treat our waste, which is about 3% of the total electricity used nationwide,” he said. But by harnessing what Ren calls “bug power,” it may be possible to turn that process into a net energy gain. Ren is also exploring the technology to clean up fracking liquid.
Other applications include water desalination, remote sensing, soil remediation, and even biocomputing.
As for Nealson, his hope is that microbe-powered water-treatment systems can be deployed in the third world as a renewable source of fresh water, using designs that maximize water recovery rather than power.
But researchers don’t have to be engineers to experience “bug power.” Microbial fuel cells are increasingly popular teaching aids in undergraduate laboratories, said Bond. “It’s just the coolest thing you’ve ever seen. It doesn’t get old.”
1. Bond, D.R., Holmes, D.E., Tender, L.M., and D.R. Lovley. 2002. Electrode-reducing microorganisms harvesting energy from marine sediments. Science. 295:483-485.
2. Myers C.R. and Nealson K.H. 1988. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science, 240:1319-21.
3. Malvankar N.S., Yalcin S.E., Tuominen M.T., and Lovley D.R. 2014. Visualization of charge propagation along individual pili proteins using ambient electrostatic force microscopy. Nature Nanotechnology, doi: 10.1038/nnano.2014.236. [Epub ahead of print]
4. Rotaru, et al., 2014. A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ Sci, 7:408-15.