A single eubacterial origin of eukaryotic pyruvate : ferredoxin oxidoreductase genes: Implications for the evolution of anaerobic eukaryotes

The iron sulfur protein pyruvate:ferredoxin oxidoreductase (PFO) is central to energy metabolism in amitochondriate eukaryotes, including those with h ydrogenosomes. Thus, revealing the evolutionary history of PFO is critical to understanding the origin(s) of eukaryote anaerobic energy metabolism. We determined a complete PFO sequence for Spironucleus barkhanus, a large fra gment of a PFO sequence from Clostridium pasteurianum, and a fragment of a new PFO from Giardia lamblia. Phylogenetic analyses of eubacterial and euka ryotic PFO genes suggest a complex history for PFO, including possible gene duplications and horizontal transfers among eubacteria. Our analyses favor a common origin for eukaryotic cytosolic and hydrogenosomal PFOs from a si ngle eubacterial source, rather than from separate horizontal transfers as previously suggested. However, with the present sampling of genes and speci es, we were unable to infer a specific eubacterial sister group for eukaryo tic PFO. Thus, we find no direct support for the published hypothesis that the donor of eukaryote PFO was the common alpha-proteobacterial ancestor of mitochondria and hydrogenosomes. We also report that several fungi and pro tists encode proteins with PFO domains that are likely monophyletic with PF Os from anaerobic protists. In Saccharomyces cerevisiae, PFO domains combin e with fragments of other redox proteins to form fusion proteins which part icipate in methionine biosynthesis. Our results are consistent with the vie w that PFO, an enzyme previously considered to be specific to energy metabo lism in amitochondriate protists, was present in the common ancestor of con temporary eukaryotes and was retained, wholly or in part, during the evolut ion of oxygen-dependent and mitochondrion-bearing lineages.