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‘Electric Mud’ Teems With New, Mysterious Bacteria
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‘Electric mud’ teems with new, mysterious bacteria [sciencemag.org]:
For Lars Peter Nielsen, it all began with the mysterious disappearance of hydrogen sulfide. The microbiologist had collected black, stinky mud from the bottom of Aarhus Harbor in Denmark, dropped it into big glass beakers, and inserted custom microsensors that detected changes in the mud’s chemistry. At the start of the experiment, the muck was saturated with hydrogen sulfide—the source of the sediment’s stink and color. But 30 days later, one band of mud had become paler, suggesting some hydrogen sulphide had gone missing. Eventually, the microsensors indicated that all of the compound had disappeared. Given what scientists knew about the biogeochemistry of mud, recalls Nielsen, who works at Aarhus University, “This didn’t make sense at all.”
The first explanation, he says, was that the sensors were wrong. But the cause turned out to be far stranger: bacteria that join cells end to end to build electrical cables able to carry current up to 5 centimeters through mud. The adaptation, never seen before in a microbe, allows these so-called cable bacteria to overcome a major challenge facing many organisms that live in mud: a lack of oxygen. Its absence would normally keep bacteria from metabolizing compounds, such as hydrogen sulfide, as food. But the cables, by linking the microbes to sediments richer in oxygen, allow them to carry out the reaction long distance.
When Nielsen first described the discovery in 2009, colleagues were skeptical. Filip Meysman, a chemical engineer at the University of Antwerp, recalls thinking, “This is complete nonsense.” Yes, researchers knew bacteria could conduct electricity, but not over the distances Nielsen was suggesting. It was “as if our own metabolic processes would have an effect 18 kilometers away,” says microbiologist Andreas Teske of the University of North Carolina, Chapel Hill.
But the more researchers have looked for “electrified” mud, the more they have found it, in both saltwater and fresh. They have also identified a second kind of mud-loving electric microbe: nanowire bacteria, individual cells that grow protein structures capable of moving electrons over shorter distances. These nanowire microbes live seemingly everywhere—including in the human mouth.
The discoveries are forcing researchers to rewrite textbooks; rethink the role that mud bacteria play in recycling key elements such as carbon, nitrogen, and phosphorus; and reconsider how they influence aquatic ecosystems and climate change. Scientists are also pursuing practical applications, exploring the potential of cable and nanowire bacteria to battle pollution and power electronic devices (see sidebar below). “We are seeing way more interactions within microbes and between microbes being done by electricity,” Meysman says. “I call it the electrical biosphere.”
Most cells thriveby robbing electrons from one molecule, a process called oxidation, and donating them to another molecule, usually oxygen—so-called reduction. Energy harvested from these reactions drives the other processes of life. In eukaryotic cells, including our own, such “redox” reactions take place on the inner membrane of the mitochondria, and the distances involved are tiny—just micrometers. That is why so many researchers were skeptical of Nielsen’s claim that cable bacteria were moving electrons across a span of mud equivalent to the width of a golf ball.
The vanishing hydrogen sulfide was key to proving it. Bacteria produce the compound in mud by breaking down plant debris and other organic material; in deeper sediments, hydrogen sulfide builds up because there is little oxygen to help other bacteria break it down. Yet, in Nielsen’s laboratory beakers, the hydrogen sulfide was disappearing anyway. Moreover, a rusty hue appeared on the mud’s surface, indicating that an iron oxide had formed.
One night, waking from his sleep, Nielsen came up with a bizarre explanation: What if bacteria buried in the mud were completing the redox reaction by somehow bypassing the oxygen-poor layers? What if, instead, they used the ample supplies of hydrogen sulfide as an electron donor, then shuttled the electrons upward to the oxygen-rich surface? There, the oxidation process would produce rust if iron was present.
Finding what was carrying these electrons proved complicated. First, Nils Risgaard-Petersen on Nielsen’s team had to rule out a simpler possibility: that metallic particles in the sediment were shuttling electrons to the surface and causing the oxidation. He accomplished that by inserting a layer of glass beads, which don’t conduct electricity, into a column of mud. Despite that obstacle, the researchers still detected an electric current moving through the mud, suggesting metallic particles were not the conductor.
To see whether some kind of cable or wire was ferrying electrons, the researchers next used a tungsten wire to make a horizontal slice through a column of mud. The current flickered out, as if a wire had been snipped. Other work narrowed down the conductor’s size, suggesting it had to be at least 1 micrometer in diameter. “That’s the conventional size for bacteria,” Nielsen says.
Ultimately, electron micrographs revealed a likely candidate: long, thin, bacterial filaments that appeared in the layer of glass beads inserted in the beakers filled with the Aarhus Harbor mud. Each filament was composed of a stack of cells—up to 2000—encased in a ridged outer membrane. In the space between that membrane and the stacked cells, many parallel “wires” stretched the length of the filament. The cablelike appearance inspired the microbe’s common name.
Meysman, the one-time skeptic, quickly became a convert. Not long after Nielsen announced his discovery, Meysman decided to examine one of his own marine mud samples. “I noticed the same color changes in the sediment that he saw,” Meysman recalls. “It was an instruction from Mother Nature to take this more seriously.”
His team began to develop tools and techniques for investigating the microbes, sometimes working collaboratively with Nielsen’s group. It was tough going. The bacterial filaments tended to degrade quickly once isolated, and standard electrodes for measuring currents in small conductors didn’t work. But once the researchers learned how to pick out a single filament and quickly attach a customized electrode, “We saw really high conductivity,” Meysman says. The living cables don’t rival copper wires, he says, but they are on par with conductors used in solar panels and cellphone screens, as well as the best organic semiconductors.
The researchers also dissected the cable bacteria’s anatomy. Using chemical baths, they isolated the cylindrical sheath, finding it holds 17 to 60 parallel fibers, glued along the inside. The sheath is the source of the conductance, Meysman and colleagues reported last year in Nature Communications. Its exact composition is still unknown, but could be protein-based.
