Electron highway for hydrogen and carbon dioxide storage discovered

FRANKFURT/MARBURG/BASEL. In 2013, a team of microbiologists led by Professor Volker Müller of Goethe University Frankfurt discovered an unusual enzyme in heat-loving (thermophilic) bacteria: hydrogen-dependent CO.₂ HDCR reductase. It produces formic acid (formic) from hydrogen gas (H₂) and carbon dioxide (CO₂), and in the process, hydrogen transfers electrons to carbon dioxide. This makes HDCR the first known enzyme to directly utilize hydrogen. On the other hand, all the enzymes known to date that produce formic acid took a detour: they obtained electrons from soluble cellular electron transfer agents, which for their part accepted electrons from hydrogen with the help of other enzymes.

The bacterium Thermoanaerobacter kivui thrives away from oxygen, for example in the deep ocean, and uses CO₂ and hydrogen to produce cellular energy. HDCR from Thermoanaerobacter kivui consists of four protein modules: one that cleaves hydrogen, one that produces formic acid and two small modules containing ferrous sulfur. “It was clear to us after our discovery that it must be two small subunits that transfer electrons from one module to another,” said Müller. In 2016, researchers observed that enzymes form long filaments. Müller: “We can see how important this structure is from the fact that filament formation massively stimulates enzyme activity.”

Researchers from Goethe University Frankfurt, together with a group led by Dr. Jan Schuller, University of Marburg and the LOEWE Center for Synthetic Microbiology, have now produced a molecular close-up of the enzyme. Through cryo-electron microscopy analysis, the Schuller group has succeeded in determining the structure of HDCR at atomic resolution. This makes the details of long filaments visible, which are formed by enzymes under experimental conditions in the laboratory (in vitro): the backbone of the filament consists of two tiny HDCR subunits, which are arranged together to form a kind of nanowire with thousands of electron-conducting iron atoms. “This is the only enzymatically decorated nanowire found so far. On this wire, the hydrogenase module and the formate dehydrogenase module sit like mushroom heads on top of the wire,” explains Schuller.

Helge Dietrich, a doctoral researcher in Volker Müller’s group at Goethe University Frankfurt, tested a genetic modification of a small module that prevents HDCR filament formation. The result: the individual components or monomers are much less active than the filament.

Enzyme monomers organize themselves into filamentous structures inside the bacterial cell as well. Professor Ben Engel, a structural cell biologist at the University of Basel, and his team contributed to these findings by performing cryo-electron tomography. Using this cutting-edge technique, the researchers discovered something special: “Hundreds of filaments are fused together to form a ring-shaped superstructure. This structure is striking—we informally call it a ‘portal’,” explains Engel. The tufts are clearly anchored to the inner membrane of the bacterial cell and span almost its entire width. Dr. Ricardo Righetto, senior scientist on Ben Engel’s team, analyzed the structure of HDCR filaments in native bacteria: “Cryo-electron tomography allows us to look directly into cells at very high resolution. Using this approach, we were really surprised to not only confirm the presence of HDCR filaments in the cells, but also to find them forming large bundles that adhere to the membrane.”

This structure reveals why the HDCR enzyme is more efficient than all chemical catalysts and much better than all known enzymes in producing formic acid as a “liquid organic hydrogen carrier” from hydrogen and CO.₂ (cf. background information). Volker Müller: “The concentration of hydrogen in this bacterial ecosystem is low, and, in addition, CO₂ and H₂ concentration can change. Filament formation and bundling not only substantially increase the concentration of this enzyme in the cell. The thousands of electron-conducting iron atoms in these ‘nanowires’ can also store electrons from intermediate hydrogen oxidation when even just a single hydrogen bubble passes through the bacteria.”

The team believes that not all of the puzzles surrounding the HDCR enzyme have not been solved through the atomic resolution of the structure. Jan Schuller said: “We don’t yet know how wires store electrons, why filament formation stimulates enzymatic activity so intensively or how the bonds are anchored in the membrane. We are working on this research question.” But the future of HDCR could be very exciting, Volker Müller believes: “Perhaps one day we will be able to produce synthetic nanowires that we can use to capture CO₂ from the atmosphere. We are also one step closer now to biological hydrogen storage.”

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