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September 13, 2018

Common Diarrhea-Causing Bacterium Found to Produce Electricity

Listeria bacteria transport electrons through their cell wall into the environment as tiny currents, assisted by ubiquitous flavin molecules (yellow dots). [Amy Cao graphic. ©UC Berkeley]

  • Researchers at the University of California (UC), Berkeley, say they have discovered that a common diarrhea-causing bacterium, Listeria monocytogenes, produces electricity using an entirely different method from known electrogenic bacteria, and that hundreds of other bacterial species use this same process. Their study (“A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria”), published online in Nature, will be good news for those currently trying to create living batteries from microbes. Such "green" bioenergetic technologies could, for example, generate electricity from bacteria in waste treatment plants.

    “Extracellular electron transfer (EET) describes microbial bioelectrochemical processes in which electrons are transferred from the cytosol to the exterior of the cell.  Mineral-respiring bacteria use elaborate haem-based electron transfer mechanisms but the existence and mechanistic basis of other EETs remain largely unknown. Here we show that the food-borne pathogen Listeria monocytogenes uses a distinctive flavin-based EET mechanism to deliver electrons to iron or an electrode. By performing a forward genetic screen to identify L. monocytogenes mutants with diminished extracellular ferric iron reductase activity, we identified an eight-gene locus that is responsible for EET. This locus encodes a specialized NADH dehydrogenase that segregates EET from aerobic respiration by channeling electrons to a discrete membrane-localized quinone pool. Other proteins facilitate the assembly of an abundant extracellular flavoprotein that, in conjunction with free-molecule flavin shuttles, mediates electron transfer to extracellular acceptors,” write the investigators.

    “This system thus establishes a simple electron conduit that is compatible with the single-membrane structure of the gram-positive cell. Activation of EET supports growth on non-fermentable carbon sources, and an EET mutant exhibited a competitive defect within the mouse gastrointestinal tract. Orthologues of the genes responsible for EET are present in hundreds of species across the Firmicutes phylum, including multiple pathogens and commensal members of the intestinal microbiota, and correlate with EET activity in assayed strains. These findings suggest a greater prevalence of EET-based growth capabilities and establish a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease.”

    Many of these sparking bacteria are part of the human gut microbiome, and many, like the bug that causes the food-borne illness listeriosis, which can also cause miscarriages, are pathogenic. The bacteria that cause gangrene (Clostridium perfringens) and hospital-acquired infections (Enterococcus faecalis) and some disease-causing streptococcus bacteria also produce electricity. Other electrogenic bacteria, like Lactobacilli, are important in fermenting yogurt, and many are probiotics.

    “The fact that so many bugs that interact with humans, either as pathogens or in probiotics or in our microbiota or involved in fermentation of human products, are electrogenic—that had been missed before," says Dan Portnoy, Ph.D., a UC Berkeley professor of molecular and cell biology and of plant and microbial biology. "It could tell us a lot about how these bacteria infect us or help us have a healthy gut."

    Bacteria generate electricity to remove electrons produced during metabolism and support energy production. Whereas animals and plants transfer their electrons to oxygen inside the mitochondria of every cell, bacteria in environments with no oxygen, including our gut, but also alcohol and cheese fermentation vats and acidic mines, have to find another electron acceptor. In geologic environments, that has often been a mineral, e.g., iron or manganese, outside the cell. In some sense, these bacteria "breathe" iron or manganese.

    Transferring electrons out of the cell to a mineral requires a cascade of special chemical reactions, the so-called extracellular electron transfer chain, which carries the electrons as a tiny electrical current. Some scientists have tapped that chain to make a battery: stick an electrode in a flask of these bacteria and you can generate electricity.

    The newly discovered extracellular electron transfer system is actually simpler than the already known transfer chain, and seems to be used by bacteria only when necessary, perhaps when oxygen levels are low, according to the research team. So far, this simpler electron transfer chain has been found in bacteria with a single cell wall—microbes classified as gram-positive bacteria—that live in an environment with lots of flavin, which are derivatives of vitamin B2. 

    "It seems that the cell structure of these bacteria and the vitamin-rich ecological niche that they occupy makes it significantly easier and more cost effective to transfer electrons out of the cell," says first author Sam Light, Ph.D., a postdoctoral fellow. "Thus, we think that the conventionally studied mineral-respiring bacteria are using extracellular electron transfer because it is crucial for survival, whereas these newly identified bacteria are using it because it is 'easy.'"

    To see how robust this system is, Dr. Light teamed up with Caroline Ajo-Franklin, Ph.D., staff scientist at Lawrence Berkeley National Laboratory, who explores the interactions between living microbes and inorganic materials for possible applications in carbon capture and sequestration and bio-solar energy generation. She used an electrode to measure the electric current that streams from the bacteria—up to 500 microamps—confirming that it is indeed electrogenic. In fact, they make about as much electricity—some 100,000 electrons per second per cell—as known electrogenic bacteria.

    Dr. Light is particularly intrigued by the presence of this system in Lactobacillus, bacteria crucial to the production of cheese, yogurt, and sauerkraut. Perhaps, he suggests, electron transport plays a role in the taste of cheese and sauerkraut.

    "This is a whole big part of the physiology of bacteria that people didn't realize existed, and that could be potentially manipulated," he says.

    Drs. Light and Portnoy have many more questions about how and why these bacteria developed such a unique system, e.g., simplicity, it's easier to transfer electrons through one cell wall rather than through two, and opportunity, taking advantage of ubiquitous flavin molecules to get rid of electrons appear to have enabled these bacteria to find a way to survive in both oxygen-rich and oxygen-poor environments.

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