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Structure paper

TitleMolecular principles of redox-coupled sodium pumping of the ancient Rnf machinery.
Journal, issue, pagesNat Commun, Vol. 16, Issue 1, Page 2302, Year 2025
Publish dateMar 7, 2025
AuthorsAnuj Kumar / Jennifer Roth / Hyunho Kim / Patricia Saura / Stefan Bohn / Tristan Reif-Trauttmansdorff / Anja Schubert / Ville R I Kaila / Jan M Schuller / Volker Müller /
PubMed AbstractThe Rnf complex is the primary respiratory enzyme of several anaerobic prokaryotes that transfers electrons from ferredoxin to NAD and pumps ions (Na or H) across a membrane, powering ATP synthesis. ...The Rnf complex is the primary respiratory enzyme of several anaerobic prokaryotes that transfers electrons from ferredoxin to NAD and pumps ions (Na or H) across a membrane, powering ATP synthesis. Rnf is widespread in primordial organisms and the evolutionary predecessor of the Na-pumping NADH-quinone oxidoreductase (Nqr). By running in reverse, Rnf uses the electrochemical ion gradient to drive ferredoxin reduction with NADH, providing low potential electrons for nitrogenases and CO reductases. Yet, the molecular principles that couple the long-range electron transfer to Na translocation remain elusive. Here, we resolve key functional states along the electron transfer pathway in the Na-pumping Rnf complex from Acetobacterium woodii using redox-controlled cryo-electron microscopy that, in combination with biochemical functional assays and atomistic molecular simulations, provide key insight into the redox-driven Na pumping mechanism. We show that the reduction of the unique membrane-embedded [2Fe2S] cluster electrostatically attracts Na, and in turn, triggers an inward/outward transition with alternating membrane access driving the Na pump and the reduction of NAD. Our study unveils an ancient mechanism for redox-driven ion pumping, and provides key understanding of the fundamental principles governing energy conversion in biological systems.
External linksNat Commun / PubMed:40055346 / PubMed Central
MethodsEM (single particle)
Resolution2.8 - 3.3 Å
Structure data

19915

9eri

EMDB-19915, PDB-9eri:
Cryo-EM structure of sodium pumping Rnf complex from Acetobacterium woodii bound to NADH
Method: EM (single particle) / Resolution: 3.3 Å

19916

9erj

EMDB-19916, PDB-9erj:
Cryo-EM structure of sodium pumping Rnf complex from Acetobacterium woodii reduced with low potential Ferredoxin
Method: EM (single particle) / Resolution: 2.9 Å

19919

9erk

EMDB-19919, PDB-9erk:
Cryo-EM structure of sodium pumping Rnf complex from Acetobacterium woodii reduced with low potential ferredoxin (consensus map)
Method: EM (single particle) / Resolution: 2.8 Å

19920

9erl

EMDB-19920, PDB-9erl:
Cryo-EM structure of sodium pumping Rnf complex from Acetobacterium woodii in apo state
Method: EM (single particle) / Resolution: 3.0 Å

Chemicals

ChemComp-FES:
FE2/S2 (INORGANIC) CLUSTER

ChemComp-SF4:
IRON/SULFUR CLUSTER

ChemComp-FMN:
FLAVIN MONONUCLEOTIDE

ChemComp-NAD:
NICOTINAMIDE-ADENINE-DINUCLEOTIDE / NAD*YM

ChemComp-RBF:
RIBOFLAVIN

ChemComp-NA:
Unknown entry

Source
  • acetobacterium woodii dsm 1030 (bacteria)
KeywordsMEMBRANE PROTEIN / Bioenergetics / anaerobic cryoEM / electron transport / redox-driven sodium pumping / Anaerobic metabolism / electron transfer / sodium pumping

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