Electron Life – Seeking biological electron transfer in the field of electro-microbiology

How would you express the theme of your work?

Ryuhei Nakamura

D.Sci.

Team Leader
Biofunctional Catalyst Research Team

I am a physical chemist and the electron is the key word for my field. I am trying to understand the trials of nature in the course of becoming accustomed to different environments from the view point of “electron flow" (Fig. 1). This history of geological and biological electron flow is a great textbook, a blueprint for us to predict the future. We can learn a lot from the evolution, and it takes the field of biology and geology together. I think overall understanding of nature’s evolution is needed, rather than trying to understand each specific step in detail, and such a comprehensive approach will provide the new guiding principle for us to design the catalysts and develop the technology for energy and environmental conservation in human society.

Fig.1 Electron Flow & Evolution of Life
Our target is to find the role of electrical current for emergence and evolution of life; how nature has utilized the electrical current from billion years ago, and its relevance in our modem technology, such as fuel cell, battery, voltage amplifier, and thermoelectric conversion. Knowing the evolution of this in nature would be a nice guidance to realize sustainable human ecosystems. © R. Nakamura

How would you describe your Laboratory and working in CSRS at RIKEN?

I joined the center in April 2013, as one of the new Principal Investigators at CSRS from outside of RIKEN. The topic of Sustainability was the attraction for me. Here in my lab, we have about 10 people in our team. With the members who have the diverse backgrounds from physical chemistry to microbiology, I am trying to combine those areas to understand the fundamental mechanisms of nature to organize the robust and efficient energy cycle. I am sure its sustainability is relevant to modern technologies in human society.

RIKEN is a very special place, with so many outstanding scientists. There is a great freedom of what to research and we can focus basic subjects and cultivate frontier science. In our center, distinguished researchers of plant science, chemical biology, biomass, and chemistry work together. Especially for young scientists, collaborating between the different fields and heavyweight experienced researchers is a very great incentive, since it helps them a lot to come up with the brand-new ideas, and they can even make their own field. Also for me this collaboration is quite attractive, and has encouraged me a lot to establish my own vision.

What are some of the interesting research projects you are working on?

We work on the development of biologically inspired catalysts and their application for energy harvesting and environmental conservation systems. Specifically, we attempt to exploit the nature’s ingenuities of multi-electron catalytic reaction, electron/proton transport, metabolic regulation, flexible response to external stimuli, and the robust energy management in a deep sea environment to develop the novel materials and systems necessary for the effective management of renewable energy sources. There are three areas for our research:

1. Investigation of giant electro ecosystems in a deep hydrothermal environment
2. Electricity conversion by the microbial ability of extracellular electron transfer
3. Development of catalysts for water oxidation, inspired by the biological mechanism and reactions in plants such as natural photosynthesis

Could you tell us about these Electro-Ecosystems?

Fig.2  Chimney: Giant Electrochemical Fuel Cell Sustained by Magmatic Activity?
The chemical potential and temperature gradient across the chimney generates electrical current, which trigger abiotic CO2 reduction and may sustain the ecosystems of the chimney.

In 2010 we published the first paper about electricity generation in the deep sea hydrothermal vent (Ref.1). We were the first to propose and demonstrate that a black smoker chimney acts as an electrochemical fuel cell that can convert the energy stored in the earth’s interior to electricity (Fig. 2).

Our research has also inspired another field of the origin of life (Ref.2). This field has a quite long history, and the difficult point of this field is that we always have to investigate about the past events occurred billions of years ago. So, in order to get to the conclusive point of view, a broad range of understanding in physical chemistry, biology, and geology are required to understand the framework.

But always the problem has been that for some (sub) surface regions in the deep sea there is no recognizable energy input. There is no sunlight. There is no energy to sustain the bacterial activity we see. So people are looking for what is the energy source to sustain such an abundant biomass in the sub sea floor. So I am quite sure that this source has become the electron. Now in the field of Earth science people started to recognize Electro-microbiology, and the electrochemical fuel cell in the deep ocean as a kind of power and engine to maintain the microbial activity.

We think that this energy creation found in the deep sea electro-ecosystem could have been one of the sources to kick-off the origin of life. The gradient of redox and temperature around a chimney creates electrical energy, which could kick off chemical evolution. This type of electrical energy might be the third type of ecosystem, in addition to chemosynthesis and photosynthesis, to drive microbial life (Fig. 3 / Ref.4).

Fig.3 Ecosystems Sustained by Geo-electricity
Decoupling of electron and heat transfer can generate the high energy electron that has almost the same electrochemical potential generatedby photosynthesis.

I want to know how nature got accustomed to the different environments, and how organisms in nature overcame such quite difficult situations by changing their metabolism or changing their genome. For example, it is as if chimney minerals have such an advanced knowledge of physics: they can convert chemical energy to electricity, and electricity to chemical energy. Such an amazing function can be a key to generate high energy electrons, for triggering CO2 fixation, and nitrogen fixation in the ancient deep sea.

We also found another amazing aspect of chimney minerals: by analyzing the samples of minerals from the deep sea and investigating the function of them with Dr. Takao Mori of National Institute for Materials Science, we found that they transfer electrons efficiently, but not heat energy (Ref.3). It represents a newly recognized system for energy-harvesting in nature, based on the decoupling of electron transfer and heat transfer. No one would imagine this! I would say that at the hydrothermal vent the difference of chemical potential and temperature is converted to electrical current, and if proton motive force exists, a hydrothermal vent can generate reductive energy almost identical with that of photo-excited photosynthesis II. This is a new scenario to bridge deep-sea ecosystem and photosynthesis in terms of energetics for carbon fixation, and recently published in a book chapter (Ref.4). This is one of our original discoveries and can be a basis for examining the relationship between modern technology and ancient one in respect to heat and electrical use.

How is electrical energy actually transferred and used by organisms in their metabolisms?

The next challenge for us is to test our hypothesis on the newly understood type of bacteria called “Electrotrophs” in which CO2 fixation is triggered by electrons taken from minerals or electrodes.

Scientists in the USA (Prof. Kenneth Nealson and Prof. Derek Lovely) noticed that certain bacteria transferred electron from some minerals like iron oxide or manganese oxide, as a process for their respiration. Those findings were the starting point of the new field of electro-microbiology. Usually we need oxygen for respiration, and mitochondria plays a role. But even without oxygen some bacteria eat minerals to maintain their ATP synthesis. Some portion of bacteria, archaea and animals depend on this kind of energy metabolism.

The current goal of our research is to prove the concept of such “electro-ecosystems” both by lab experiments and on-site deep-sea experiments (Fig. 4 / Ref.5). People will recognize the importance of this field soon. Electron life might be a nice running title - the field of electron Life.

Fig.4 From Chemolithoautroph to Electrolithoautotroph

REFERENCES

1. Nakamura, R., Takashima, T., Kato, S., Takai, K., Yamamoto, M., Hashimoto, K.
Electrical Current Generation across a Black Smoker Chimney.
Angew. Chem.Int. Ed. 49, 7692-7694 (2010) *Selected to Hot Topics in Sustainable Chemistry
DOI: 10.1002/anie.201003311
   
2. Yamaguchi, A., Yamamoto, M., Takai, K., Ishii, T., Hashimoto, K., Nakamura, R.
Electrochemical CO2 Reduction by Ni-containing Iron Sulfides: How Is CO2 Electrochemically Reduced at Bisulfide-Bearing Deep-sea Hydrothermal Precipitates?
Electrochemica Acta 141, 311-318 (2014)
DOI: 10.1016/j.electacta.2014.07.078
   
3. Ang, R., Khan, A., Tsujii, N., Takai, K., Nakamura, R., Mori, T.
Thermoelectricity Generation and Electron-Magnon Scattering in a Natural Chalcopyrite Mineral from a Deep-Sea Hydrothermal Vent.
Angew. Chem. 54, 12909-12913 (2015)
DOI:10.1002/anie.201505517
   
4. Yamaguchi, A., Li, Y., Takashima, T., Hashimoto, K., Nakamura, R.
CO2 Reduction Using an Electrochemical Approach from Chemical, Biological, and Geological Aspects in the Ancient and Modern Earth.
Solar to Chemical Energy Conversion, 32, 213-228 (2016)
   
5. Ishii, T., Kawaichi, S., Nakagawa, H., Hashimoto, K., Nakamura, R.
From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources.
Front. Microbiol., 6, 994 (2015)
DOI: 10.3389/fmicb.2015.00994
   
6. RIKEN News: A bacteria's double life: living off both iron and electricity (Dec. 2015)
   
7. RIKEN It Ain’t Magic: Black smokers and Electro-ecosystems (Dec 27, 2015)
   
8. RIKEN It Ain’t Magic: Electrolithoautotrophs (Jan 13, 2016)