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 hydrogenosomes. 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 fragment of a PFO sequence from Clostridium pasteurianum, and a fragment of a new PFO from Giardia lamblia. Phylogenetic analyses of eubacterial and eukaryotic 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 single eubacterial source, rather than from separate horizontal transfers as previously suggested. However, with the present sampling of genes and species, we were unable to infer a specific eubacterial sister group for eukaryotic 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 protists encode proteins with PFO domains that are likely monophyletic with PFOs from anaerobic protists. In Saccharomyces cerevisiae, PFO domains combine with fragments of other redox proteins to form fusion proteins which participate in methionine biosynthesis. Our results are consistent with the view that PFO, an enzyme previously considered to be specific to energy metabolism in amitochondriate protists, was present in the common ancestor of contemporary eukaryotes and was retained, wholly or in part, during the evolution of oxygen-dependent and mitochondrion-bearing lineages.
Horner
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Department of Zoology, Natural History Museum, London, England.
Hirt
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Embley
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D000693:Anaerobiosis; D000818:Animals; D001483:Base Sequence; D003013:Clostridium / Q000201:enzymology / Q000235:genetics; D017931:DNA Primers / Q000235:genetics; D016828:Diplomonadida / Q000201:enzymology / Q000235:genetics; D005057:Eukaryotic Cells; D019143:Evolution, Molecular; D020440:Gene Duplication; D022761:Gene Transfer, Horizontal; D005798:Genes, Bacterial; D017125:Genes, Protozoan; D016829:Giardia lamblia / Q000201:enzymology / Q000235:genetics; D007658:Ketone Oxidoreductases / Q000235:genetics*; D008957:Models, Genetic; D008969:Molecular Sequence Data; D010802:Phylogeny; D050743:Pyruvate Synthase
D017931:DNA Primers; D007658:Ketone Oxidoreductases; D050743:Pyruvate Synthase