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

Anja Poehlein,Gerhard Gottschalk,Meike Goenrich,John Vollmers,Johannes Bertsch,Michael Hecker,Rolf Daniel,Birgit Voigt,Andrea Thürmer,Volker Müller,Kai Schuchmann,Silke Schmidt,Rudolf K Thauer,Anne-Kristin Kaster

doi:10.1371/journal.pone.0033439

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.

Highlights

The atmosphere in the early days of our planet was highly reducing and did not contain oxygen but gases such as molecular hydrogen and carbon dioxide
The genome of A. woodii consists of a single circular 4,044,785 bp chromosome with a GC content of 39.3%. 3473 protein-encoding ORFs, 5 rRNA clusters and 60 tRNA genes account for 85.1% of the genomic DNA. 71.1% of the predicted ORFs are with assigned functions (NCBI database, accession number CP002987)
The acetogenic bacterium A. woodii is a prime candidate for an organism that catalyzes what may be one of the first life sustaining processes on earth based on CO2 fixation

Summary

Introduction

The atmosphere in the early days of our planet was highly reducing and did not contain oxygen but gases such as molecular hydrogen and carbon dioxide. The Wood-Ljungdahl pathway of carbon dioxide fixation is such a pathway and, could be considered to have evolved on earth very early [2,3] It is present in strictly anaerobic sulfate reducing bacteria and archaea, in methanogenic archaea and acetogenic bacteria [4]. The pathway involves reduction of carbon dioxide to formate, binding of formate to the cofactor tetrahydrofolate (THF) and subsequent reduction of the formyl group to methyl tetrahydrofolate Another mol of carbon dioxide is reduced to enzymetrapped carbon monoxide that is condensed with a methyl group and coenzyme A to yield acetyl- CoA (Fig. 1). The amount of energy gained from equation 1 would theoretically allow the generation of only 1.5 mol of ATP per mol acetate produced [8] This calculation is based on a partial pressure of molecular hydrogen of 1 bar. Acetogens clearly live at the thermodynamic limit of life

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Conclusion