Ferredoxin reduction by hydrogen with iron functions as an evolutionary precursor of flavin-based electron bifurcation

• 成果类型: Article
• 署名作者: Brabender, Max; Pereira, Delfina P. Henriques; Mrnjavac, Natalia; Schlikker, Manon Laura; Kimura, Zen-Ichiro; Sucharitakul, Jeerus; Kleinermanns, Karl; Tueysuez, Harun; Buckel, Wolfgang; Preiner, Martina; Martin, William F.
• 署名单位: Heinrich Heine University Dusseldorf; Max Planck Society; Philipps University Marburg; Chulalongkorn University; Heinrich Heine University Dusseldorf; Max Planck Society; Max Planck Society; Philipps University Marburg; Philipps University Marburg
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-14693
• DOI: 10.1073/pnas.2318969121
• 发表日期: 2024-03-19
• 关键词: ENERGY-CONSERVATION; origin; LIFE; dehydrogenase; serpentinite; mechanism; clusters; insights; archaea; complex

摘要

Autotrophic theories for the origin of metabolism posit that the first cells satisfied their carbon needs from CO2 and were chemolithoautotrophs that obtained their energy and electrons from H2. The acetyl-CoA pathway of CO2 fixation is central to that view because of its antiquity: Among known CO2 fixing pathways it is the only one that is i) exergonic, ii) occurs in both bacteria and archaea, and iii) can be functionally replaced in full by single transition metal catalysts in vitro. In order to operate in cells at a pH close to 7, however, the acetyl-CoA pathway requires complex multi- enzyme systems capable of flavin-based electron bifurcation that reduce low potential ferredoxin-the physiological donor of electrons in the acetyl-CoA pathway-with electrons from H2. How can the acetyl-CoA pathway be primordial if it requires flavin-based electron bifurcation? Here, we show that native iron (Fe0), but not Ni0, Co0, Mo0, NiFe, Ni2Fe, Ni3Fe, or Fe3O4, promotes the H2 - dependent reduction of aqueous Clostridium pasteurianum ferredoxin at pH 8.5 or higher within a few hours at 40 degrees C, providing the physiological function of flavin-based electron bifurcation, but without the help of enzymes or organic redox cofactors. H2 - dependent ferredoxin reduction by iron ties primordial ferredoxin reduction and early metabolic evolution to a chemical process in the Earth's crust promoted by solid - state iron, a metal that is still deposited in serpentinizing hydrothermal vents today.