Premium
Role of geochemical protoenzymes (geozymes) in primordial metabolism: specific abiotic hydride transfer by metals to the biological redox cofactor NAD +
Author(s) -
Henriques Pereira Delfina P.,
Leethaus Jana,
Beyazay Tugce,
Nascimento Vieira Andrey,
Kleinermanns Karl,
Tüysüz Harun,
Martin William F.,
Preiner Martina
Publication year - 2022
Publication title -
the febs journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.981
H-Index - 204
eISSN - 1742-4658
pISSN - 1742-464X
DOI - 10.1111/febs.16329
Subject(s) - nad+ kinase , hydride , cofactor , chemistry , redox , hydrogenase , nickel , inorganic chemistry , hydrogen , dehydrogenase , electron transfer , photochemistry , biochemistry , organic chemistry , enzyme
Hydrogen gas, H 2 , is generated in serpentinizing hydrothermal systems, where it has supplied electrons and energy for microbial communities since there was liquid water on Earth. In modern metabolism, H 2 is converted by hydrogenases into organically bound hydrides (H – ), for example, the cofactor NADH. It transfers hydrides among molecules, serving as an activated and biologically harnessed form of H 2 . In serpentinizing systems, minerals can also bind hydrides and could, in principle, have acted as inorganic hydride donors—possibly as a geochemical protoenzyme, a ‘geozyme’— at the origin of metabolism. To test this idea, we investigated the ability of H 2 to reduce NAD + in the presence of iron (Fe), cobalt (Co) and nickel (Ni), metals that occur in serpentinizing systems. In the presence of H 2 , all three metals specifically reduce NAD + to the biologically relevant form, 1,4‐NADH, with up to 100% conversion rates within a few hours under alkaline aqueous conditions at 40 °C. Using Henry's law, the partial pressure of H 2 in our reactions corresponds to 3.6 m m , a concentration observed in many modern serpentinizing systems. While the reduction of NAD + by Ni is strictly H 2 ‐dependent, experiments in heavy water ( 2 H 2 O) indicate that native Fe can reduce NAD + both with and without H 2 . The results establish a mechanistic connection between abiotic and biotic hydride donors, indicating that geochemically catalysed, H 2 ‐dependent NAD + reduction could have preceded the hydrogenase‐dependent reaction in evolution.