Long before we humans called planet Earth our home, it belonged to microorganisms. More than three billion years before Faraday, Maxwell and Thomson, microorganisms harnessed electricity to power their cells. The Earth was an altogether different place back then. Without oxygen to breathe, iron and sulphur compounds played a key role in microbial metabolism serving as substrates for microbial respiration. Tiny biomolecular engines harvested metals from the environment, assembled them into redox-active metalloenzymes, and began respiring iron and sulphur by breaking down hydrogen as a fuel. This process of channelling electricity between high-energy donor molecules and lower-energy acceptors is the primary mechanism for all living cells to conserve energy, move, grow and multiply. Instead of using solid metal wiring, microorganisms rely on membrane-embedded proteins containing atoms of iron, copper, or manganese that step-by-step pass electrons from one to another, with each step providing useful energy for the cell. Some microorganisms, however, did invent their own electrically conductive wires, the structures and the roles of which we only recently began to understand.

Extracellular electron transfer

In the absence of oxygen, or any other soluble electron acceptors, microorganisms face a substantial challenge: the electrons from the high-energy donors get “stuck” in the membrane proteins and no more energy can be made, unless they are discharged. In this situation, solid minerals may serve as a replacement, but they are simply too large to be taken up by the cells. Here is where microbial electrically conductive wires come into play to perform extracellular electron transfer. Extracellular electron transfer is the core concept in electromicrobiology – the field of research studying microbial electricity. Via extracellular electron transfer microbes can discharge metabolic electrons onto acceptors outside their cells, be it a mineral, another cell or an electrical device.

Although it is possible to extract electricity from virtually any microorganism, some bacteria are specialists in extracellular electron transfer and can produce biological wires that rival electrical conductivity of modern semiconductors. For instance, bacteria like Shewanella or Geobacter build long chains of protein that traverse the cell envelope, thereby connecting the inside of the cell to the outside environment. The vast majority of these bacterial nanowires – if not all – contain iron that is bound by a heme moiety, just like in human red blood cells, and can transport electrons over distances tens to hundreds of times the size of the cell itself. And some bacteria take electron conduction ever farther.

Cable bacteria

Cable bacteria Electronema and Electrothrix seemingly took a different approach to extracellular electron transfer. Instead of forming long extracellular nanowires, they form centimetrelong electrically conductive fibres. These fibres are encased under the cell envelope, and stretch the entire length of their multicellular filaments, conducting electricity from one end of the filament to the other. Being large and electrically conductive, cable bacteria attract other microorganisms and serve them as a living highway for electrons, a conductive snorkel towards oxygen, which is usually harmful to microbes that cannot tolerate its high reactivity. Here, too, metals, like iron and nickel, play an important role, but the structure of these fibres appears more complex than that of Shewanella or Geobacter nanowires. These fibres are ten times thicker than nanowires and, in addition to electrical conductivity, bestow cable bacteria an incredible toughness akin to stainless steel. Their conductivity is retained upon extraction under laboratory conditions, and they have already been successfully integrated into electrical circuits, albeit transiently.

Microbial electrochemical technologies

Just like with the invention of electricity, microorganisms evolved different mechanisms of chemical catalysis long before any industrial-scale synthesis began. In fact, they are so good at it that many of the modern production pipelines rely on microbial biotechnology. For industrial-scale electricity production, however, the situation is not yet in favour of microbial technologies. Model bacterial specialists in extracellular electron transfer require organic matter input as a source of electrons, and a lot of energy stored in these molecules is spent inside the cells of bacteria for growth and metabolic maintenance. Photosynthetic microbes, in turn, can source electrons from water, which is an accessible resource, and fix carbon dioxide from the atmosphere to grow. They, however, lack specialised electrically conductive proteins that could efficiently interface with electrodes for electricity production. So, it is an active area of electromicrobiology research to understand the electron transport pathways in microbes and how we can engineer them to perform extracellular electron transfer most efficiently. While the existing microbial electron transport pathways can be rewired with electrons intercepted and redirected with the help of redox chemistry, in theory, it is conceivable that a new-tonature chain of proteins can be engineered. As long as the right balance between the products and the substrates is maintained, and the cell can conserve energy to sustain itself, a custom pair of molecules can be coupled.

The planet of microbes

Microbial life has been, is and will remain the most successful form of life on Earth. They are responsible for the healthy functioning of all ecosystems, and their unyielding contribution to nutrient cycling that makes our planet habitable is beyond compare. These microscopic molecular factories are the most sustainable engines, capable of electrically powering themselves and transforming the environment we all live in. Even though we have come a long way since we first discovered microbial life, there is still much to learn about how to coexist with these microorganisms that, although they have no need for us, can do everything that we need.

Leonid Digel is a Carlsberg Foundation Postdoctoral Fellow at the Yusuf Hamied Department of Chemistry researching microbial electricity.

Image credit: the photograph was taken by the author in Micropia Museum. Amsterdam, the Netherlands.