An Ancient Pathway Combining Carbon Dioxide Fixation with the Generation and Utilization of a Sodium Ion Gradient for ATP Synthesis

Abstract

Synthesis of acetate from carbon dioxide and molecular hydrogen is considered to be the first carbon assimilation pathway on earth. It combines carbon dioxide fixation into acetyl-CoA with the production of ATP via an energized cell membrane. How the pathway is coupled with the net synthesis of ATP has been an enigma. The anaerobic, acetogenic bacterium Acetobacterium woodii uses an ancient version of this pathway without cytochromes and quinones. It generates a sodium ion potential across the cell membrane by the sodium-motive ferredoxin:NAD oxidoreductase (Rnf). The genome sequence of A. woodii solves the enigma: it uncovers Rnf as the only ion-motive enzyme coupled to the pathway and unravels a metabolism designed to produce reduced ferredoxin and overcome energetic barriers by virtue of electron-bifurcating, soluble enzymes.

The TP0796 Lipoprotein of Treponema pallidum Is a Bimetal-dependent FAD Pyrophosphatase with a Potential Role in Flavin Homeostasis

“…Thus, in T. pallidum and other bacteria, there very likely are periplasmic proteins that require FMN for their function. The apparent absence of quinone-synthesizing enzymes in T. pallidum (4) suggests that its Rnf components (and thus Ftp) play a critical role in energy transduction (73) in this bacterium.…”

Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin

“…Finally, transcripts of Rnf were enriched in the LI (B150 times higher than in sea water). The presence of sodium-motive ferredoxin:-NAD oxidoreductase (Rnf) subunits may indirectly indicate the presence of organisms capable of completely relying on a sodium ion potential for energetic reactions (Biegel et al, 2011;Poehlein et al, 2012). The Rnf membrane-associated electrogenic antiporter is apparently involved in generating sodium ion gradients.…”

A Bacterial Electron-bifurcating Hydrogenase

“…Instead, A. woodii employs a sodium-motive ferredoxin: NAD ϩ -oxidoreductase (Rnf complex) that couples the exergonic electron flow from reduced ferredoxin to NAD ϩ to establish a transmembrane electrochemical Na ϩ gradient that then drives the synthesis of ATP via a well characterized Na ϩ F 1 F 0 -ATP synthase (9 -15). The genome sequence showed that the Rnf complex is apparently the only ion (Na ϩ ) motive enzyme coupled with the process of acetogenesis, which underlines the importance of reduced ferredoxin for the energy metabolism of A. woodii (8).…”

“…In the anabolic route, acetyl-CoA is the precursor molecule for biosynthetic reactions (5-7). The anaerobic acetogenic bacterium Acetobacterium woodii uses a simple, ancient version of this pathway that combines carbon dioxide fixation with the generation and utilization of a sodium ion gradient across the cytoplasmic membrane for ATP synthesis (4,8). That pathway does not involve cytochromes or quinones.…”

“…Unfortunately, the enzyme(s) involved in the reaction was (were) not identified or further characterized. The genome of A. woodii encodes one monomeric [FeFe]-hydrogenase that is genetically organized in the context of the formate dehydrogenase, indicating a role in formate oxidation (8). The other hydrogenase encoded is a putative multimeric [FeFe]-hydrogenase that is present in cells grown on fructose but to 3-fold up-regulated in cells grown on H 2 ϩ CO 2 (8), indicating a role for the multimeric hydrogenase in hydrogen oxidation (8).…”