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Recently, an entirely novel type of microbial respiration has been discovered, whereby long filamentous bacteria are capable of generating and mediating electrical currents over centimeter-scale distances. On this page you can find more detailed information on why this is such a revolutionary phenomenon, turning upside down ideas in microbial ecology and sediment biogeochemistry.

nature11638-f1_2Conceptual scheme of long-range electron transport in marine sediments. Electrons are passed from cell to cell along a sequence of more than 10000 cells in a bucket brigade fashion. This results in an electrical current from the deeper sediment layers where sulfide is produced to the surface layer of the sediment where oxygen is present. Adapted from Reguera (2012, Nature 491, 201 – 202)

A surprise in the seafloor

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Long-range electron transport was originally discovered in sediment core incubations like these (Nielsen et al., Nature, 2010). The process drastically changes the biogeochemistry of the seafloor surface sediments, as indicated by the color changes in the top few centimeters.

 

In 2010, the team of Lars Peter Nielsen and Nils Risgaard-Petersen at Aarhus University discovered something incredible: bacteria that are capable of generating and conducting electrical currents over centimeter distances. This intriguing phenomenon was first observed in a series of laboratory experiments with homogenized marine sediments from the Baltic Sea (Nielsen et al. 2010). One important question was whether the process also occurs under natural conditions? Recently, our research team has been able to show that the process occurs naturally in a wide range of coastal habitats, such as coastal mud accumulation plains, salt marshes and seasonal hypoxic basins (Malkin et al. 2014). These findings show that truly new discoveries can be made within the seafloor.

A new form of microbial life

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Image of a filament obtained by Fluorescent In Situ Hybridisation.

Microorganims are capable of complex and sophisticated cooperative behaviour, as seen in quorum sensing or metabolic syntrophy. Yet, none of the recent advancements in microbial ecology has been so perplexing as the recent proposal that microorganisms are capable of electrical communication over long centimeter-scale distances.

Such electrical communication has not been seen before, and some microbiologists even call it a new form of life. Until now, the rule in biology is that each living cell generates its own biochemical energy. This rule holds for all organisms, from single celled bacteria to multicellular elephants. The energy production is localized within the cell wall, and all molecules involved in the energy metabolism (i.e. both electron donors, like sugars, and electron acceptors, like O2)  must be transported to each cell (this is why we and other animals have such an elaborate circular system).

In our filamentous electrogenic bacteria, the energy production is cooperative, and no longer occurs per individual cell. All cells within the filament are involved in the production of biochemical energy, and there is a clear separation of duties: some cells produce electrons, while other cells consume electrons. The interaction between cells occurs by sending electrons (i.e. electricity) from cell to cell.

A natural battery

The electrochemical cell was invented by Alessandro Volta in 1800, and it is generally considered to be a stroke of superb human genius. Now it is clear that micro-organisms have invented and exploited this process for millions of years. The recent discovery of long-range electron transport makes that the sediment in essence operates like an natural biogeobattery. This discovery shows how inventive the process of biological evolution can be. By creating a natural battery, these electricity generating bacteria gain an enormous advantage in the competition for sulphide, which is the electron donor for their metabolism.

A world record in microbial electron transfer

Extracellular electron transport, ranging in scale from 1 to 100 microns, is known from dissimilatory metal-reducing bacteria and from biofilms at the electrodes of microbial fuel cells. Yet, the newly proposed long-range electron transport operates on the scale of centimetres, thereby extending the known length scale of microbially mediated electron transmission by four orders of magnitude. Microscopic inspection of the sediment reveals that a network of centimeter-long filamentous bacteria spans the suboxic zone. Clever perturbation experiments recently have shown that these filamentous bacteria are responsible for the observed electron transport (Pfeffer et al., 2012).

A new avenue for biotechnological applications

This discovery also opens up a whole new avenue for applied research, and particularly, the capability of long-range microbial electron transport could stimulate novel developments in the emerging field of microbial electrocatalysis. Such novel bio-electrochemical systems potentially could lead to novel types of microbial fuel cells and electricity driven environmental remediation processes.