It’s an unlikely love story: two bacteria of different phyla, with completely opposite metabolic strategies, forming a symbiotic relationship involving electrical energy? Believe it or not, the species Geobacter sulfurreducens and Prosthecochloris aestuarii can generate an electrical current! Understanding the relationship between these two microbes has important implications for ecology, and brings scientists closer to a solar-powered, renewable form of energy.
Discovered in 1987 in a ditch in Oklahoma by UMass Amherst professor Derek Lovely, the genus Geobacter is famous for its electrogenicity, or ability to produce electrical energy. The species Geobacter sulfurreducens is capable of reducing both metal and sulfur- hence its name. (Another well-known relative is creatively named G. metallireducens). This genus’ ability to reduce metals has important applications for cleaning up pollution, discussed later on. In fact, G. sulferreducens is so famous you can buy a plushie of this microbe at about 1,000,000 times its actual size! For a great overview of Geobacter research, check out this cool video about the Lovely lab, or get the latest updates on Professor Lovely’s Twitter!
Prosthecochloris aestuarii is slightly lesser known, and was discovered in 1969 in the sediment of a Ukrainian lagoon. Its name comes from the word “prosthecae,” which is used to describe the bacterium’s appendages, or the little arms that stick out from the cell. A green sulfur bacteria, it utilizes hydrogen sulfide (H2S) or elemental sulfur (So) from the mud as a source of electrons. The fact that P. aestuarii gets its electrons from an inorganic source makes it, by definition, a “lithotroph,” as opposed to an “organotroph” like G. sulfurreducens, which uses organic (carbon-based) electron donors such as acetate (CH₃COOH).
Actually, the metabolisms of G. sulfurreducens and P. aestuarii are different in every way. The word “metabolism” is used to describe the chemical processes that an organism utilizes to sustain its own life. All life can be classified by the kind of metabolism it has. These ‘metabolic classes’ describe where an organism gets its energy, electrons, and carbon. Geobacter sulfurreducens is a chemoorganoheterotroph, meaning it gets energy from chemicals (“chemo-”), and electrons and carbon from organic molecules (“-organohetero”). If this sounds strange, you might be surprised to learn that humans are another kind of chemoorganoheterotroph!
Prosthecochloris aestuarii is a photolithoautotroph: it derives energy from sunlight (“photo-”), electrons from inorganic chemicals (“-litho-”), and carbon from carbon dioxide (“-auto”). In terms of metabolism, these two bacteria could not be more different! That’s what makes the syntrophic (“syn” = together, “trophic” = nutrition or feeding habits) relationship between these microbes so surprising- even though they have vastly different metabolisms, they help complete each other’s metabolic processes!
Image source: Hannah Rose Knapp-Broas
Image sources: Hannah Rose Knapp-Broas, Geobacter image, Prosthecochloris image
The protein nanowires extending from G. sulfurreducens were labeled (the little black dots in the image) to make them visible via transmission electron microscopy. [Image source]
A ‘protein nanowire’ made out of pilin is the last stop on the ETC of Geobacter sulfurreducens, and transports high energy electrons to an external terminal electron acceptor (panel B). In this study, iron acted as the terminal electron acceptor, and it can be seen precipitating along the protein nanowires in panel A. [Image source]
Uranium, iron, and technetium have all been identified as terminal electron acceptors for Geobacter species. This has fascinating implications for bioremediation, or the clean-up of chemical pollution using microbes. For example, previous studies have found that Geobacter species could be used to remove uranium from groundwater, where it poses a major health risk. The Navajo Nation has been particularly afflicted by uranium contamination from mining projects during the Cold War, which has been linked to cancer and kidney failure. (Although this project does not use bioremediation, donate to DigDeep to help bring clean water to the Navajo Nation!). Instead of using a metal, G. sulfurreducens is also capable of using a living organism as its terminal acceptor: P. aestuarii.
This relationship is referred to as direct interspecies electron transfer (DIET), and has been studied between various species in the microbial world. The chemistry between G. sulfurreducens and P. aestuarii is of special interest for several reasons. Firstly, microbial photolithoautotrophs like P. aestuarii are extremely important to carbon cycling. The carbon cycle simply describes the flow of carbon throughout the planet and atmosphere, beginning with photoautotrophs such as P. aestuarii or plants. These organisms are primary producers: meaning they use carbon dioxide (CO2) to make organic molecules, forming the base of the food chain. Heterotrophs such as G. sulfurreducens and humans use such organic molecules as a source of carbon. Eventually, CO2 is re-formed and released during respiration, completing the cycle.
Both G. sulfurreducens and P. aestuarii live in anaerobic, or oxygen-deprived, environments, such as sediments. Previous studies had demonstrated DIET in anaerobic environments between other species, but the relationship between G. sulfurreducens and P. aestuarii was particularly exciting to scientists. It was the first time that DIET was involved in anaerobic photosynthesis. This novel discovery, coined “syntrophic anaerobic photosynthesis,” was made by Ha et al. in 2017. The authors noted this finding could illuminate methods of energy transfer and carbon cycling in anaerobic environments, with important implications for ecology.
Syntrophic anaerobic photosynthesis might occur in many different ecosystems and involve many different species, beyond just G. sulfurreducens and P. aestuarii. Ecological niche theory states that organisms must try to find a “niche,” or a particular position within a community, in order to survive. Utilizing diverse metabolic strategies such as DIET creates new niches and thus new opportunities for survival and evolution. Further characterizing the relationship between G. sulfurreducens and P. aestuarii helps scientists understand the newly discovered metabolic strategy of syntrophic anaerobic photosynthesis, which could uncover a wealth of information about how organisms adapt to harsh or competitive environments. This would allow for a greater understanding of the intricate relationships that keep ecosystems in balance, and of the evolution of life in general.
Also of interest to scientists is that the current produced by DIET can be harnessed by humans. Microbial fuel cells (MFCs) are an exciting potential source of renewable energy. Any fuel cell involves two chambers- called the anode and the cathode- connected by a metal wire. By definition, electrons flow through the metal wire from the anode, which is electron-donating, to the cathode, which is electron-accepting. Other fuel cells, such as those that power NASA spacecraft, are powered by chemical reactions. A microbial fuel cell, however, is powered by living organisms. The source of electrons at the anode is an electron-donating species of microbe, such as G. sulfurreducens. An electron-accepting species, such as P. aestuarii, is present at the cathode. The flow of electrons from the anode to the cathode could be used as a source of electrical energy.
In 2019, Huang et al. created a microbial fuel cell with G. sulfurreducens and P. aestuarii. This was exciting because it further characterized the relationship between the two species. In this study, the researchers sought to determine if DIET between G. sulfurreducens and P. aestuarii involved a pure flow of electrons or if an intermediate electron shuttle, such as H2 or formate, was used. The work by Ha et al. in 2017 did not physically separate the two species, so this aspect of DIET was previously unclear.
These figures are from the 2017 article by Ha et al. that first described syntrophic anaerobic photosynthesis between G. sulfurreducens and P. aestuarii. In this experiment, the two species of bacteria were grown together and formed a thick biofilm, a three-dimensional bacterial community (panel C). Transmission electron microscopy revealed that the two bacteria were physically touching (panels D and E), but it remained unclear if electrons alone were necessary for DIET or if an intermediate electron carrier was involved. [Image source]
The microbial fuel cell created by Huang et al. using G. sulfurreducens and P. aestuarii placed each microbe in separate compartments, joined by a metal wire enabling electron flow and a proton-exchange membrane (PEM) allowing only protons, but no larger molecules, to pass through. Since both species were able to thrive in such a system, the ultimate conclusion to the researchers’ initial question was that electrons alone are sufficient to establish DIET- no intermediate electron shuttle was needed.
The set-up of the microbial fuel cell utilizing G. sulfurreducens at the anode and P. aestuarii at the cathode. [Image source]
Both microbes were able to establish biofilms in their respective compartments: G. sulfurreducens formed a biofilm on the anode and P. aestuarii on the cathode. At the anode, G. sulfurreducens oxidized acetate, forming CO2, and sent its leftover electrons to P. aestuarii via the metal wire. No other electron acceptors were present in the anode chamber. In the cathode chamber, P. aestuarii oxidized CO2 supplied by the researchers to create organic molecules. If nitrogen gas (N2) was supplied to the cathode instead of CO2, a negligible current was produced since P. aestuarii did not have a steady source of carbon. The researchers attributed the tiny amount of current produced to P. aestuarii utilizing small amounts of CO2 that escaped from bicarbonate in the bacterial growth medium.
Under optimal conditions, this microbial fuel cell generated a current of about 0.6 mA/m2. [Image source]
Other set-ups for the microbial fuel cell acted as controls for the experiment, as shown by the blue and purple lines at 0 mA/m2 in the above figure. The purple line represents pairing G. sulfurreducens with an abiotic cathode, and the blue line represents pairing P. aestuarii with an abiotic anode. Neither of these controls generated a current, because G. sulfurreducens did not have a terminal electron acceptor, and there was no source of electrons for P. aestuarii. Together, however, these two compatible microbes were able to generate a current of 0.6 mA/m2, the red line in the graph!
Since P. aestuarii performs photosynthesis, the cathode had to be exposed to light for a current to be generated. The anode, on the other hand, was not light sensitive and could remain in the dark. Again, no current was generated when the microbes were grown in isolation.
In this microbial fuel cell, a current was only generated when the cathode was exposed to light [Image Source]
Learning that only electrons are needed for G. sulfurreducens and P. aestuarii to grow symbiotically is an important step towards better understanding syntrophic anaerobic photosynthesis. Since this experiment was conducted in the laboratory setting of a fuel cell, a next step for researchers would be to learn how this form of DIET occurs in nature. Determining which cell structures enable P. aestuarii to take up the electrons donated by G. sulfurreducens could allow scientists to identify other species that utilize this metabolic strategy. If other species of bacteria are found to have similar structures, they too might be involved in DIET.
Although this microbial fuel cell generates an electric current, a major limitation is that the cathode is light dependent. This means that the fuel cell would need to be constantly exposed to light in order for a current to be created- making it impractical for common usage. While this particular “photo-MFC” will likely never be used by humans, it brings scientists closer to the eventual goal of renewable energy powered by microbes.
A truly remarkable photo-MFC would place the photosynthetic bacterium at the anode rather than the cathode- the opposite set-up of the MFC built using G. sulfurreducens and P. aestuarii.- so that solar energy initiated the current. Although this photo-MFC would still be light-dependent, it would harness sunlight, rather than acetate, as the initial source of energy. This would be an exciting form of renewable energy, because unlike fossil fuels or even acetate, solar energy is in indefinite supply!
For the time being, scientists will continue to explore microbial fuel cells using Geobacter species because they are so good at generating electricity, at least until the perfect photosynthetic, current-producing microbe is found. G. sulfurreducens has a high current density, or amount of charge per unit of time, making it a very efficient microbe to use at the anode of a fuel cell. Also, the ability of Geobacter species to clean-up toxins from the environment is another exciting application of this microbe, and will continue to be explored. Finally, characterizing the syntrophic relationship between two vastly different bacteria such as G. sulfurreducens and P. aestuarii will help ecologists understand the flow of electrons, energy, and carbon throughout various ecosystems.
If anything, the relationship between G. sulfurreducens and P. aestuarii confirms the age-old adage “opposites attract.” While the chemistry between these two microbes might not bring around the solar revolution, it still teaches us a lot about microbial metabolism and ecology, and makes a sweet little love story that is fun to tell at dinner parties. Thanks for reading!
About the author:
Hannah Rose Knapp-Broas '21 is a junior at Mount Holyoke College, where she studies biological sciences and reproductive health, rights, and justice. She is particularly interested in studying microbes that cause sexually transmitted diseases, and works in the Lijek Lab at MHC, which researches Chlamydia trachomatis. However, she is also interested in climate justice, and finds the prospect of environmentally-friendly microbial fuel cells exciting!
About the author:
Hannah Rose Knapp-Broas '21 is a junior at Mount Holyoke College, where she studies biological sciences and reproductive health, rights, and justice. She is particularly interested in studying microbes that cause sexually transmitted diseases, and works in the Lijek Lab at MHC, which researches Chlamydia trachomatis. However, she is also interested in climate justice, and finds the prospect of environmentally-friendly microbial fuel cells exciting!
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