MBE Advance Access published online on October 5, 2009
Molecular Biology and Evolution, doi:10.1093/molbev/msp237
Research Article |
Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes
Stechmann A. & Roger A.J. – Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, N.S., B3H 1X5
Hug L.A. – current address: Department of Cell and Systems Biology, University of Toronto, Toronto, Ontario
Corresponding author: Andrew J. Roger, Sir Charles Tupper Medical Building, 5850 College St., Halifax, NS, B3H 1X5, Tel: (902) 494-2620 Fax: (902) 494-1355, andrew.roger{at}dal.ca
Received for publication August 8, 2009. Revision received September 24, 2009. Accepted for publication September 28, 2009.
Protists that live in low oxygen conditions often oxidize pyruvate to acetate via anaerobic ATP-generating pathways. Key enzymes that commonly occur in these pathways are pyruvate:ferredoxin oxidoreductase (PFO) and [FeFe]-hydrogenase (H2ase) as well as the associated [FeFe]-H2ase maturase proteins HydE, HydF, and HydG. Determining the origins of these proteins in eukaryotes is of key importance to understanding the origins of anaerobic energy metabolism in microbial eukaryotes. We conducted a comprehensive search for genes encoding these proteins in available whole genomes and expressed sequence tag (EST) data from diverse eukaryotes. Our analyses of the presence/absence of eukaryotic PFO, [FeFe]-H2ase, and H2ase maturase sequences across eukaryotic diversity reveals orthologs of these proteins encoded in the genomes of a variety of protists previously not known to contain them. Our phylogenetic analyses revealed: (i) extensive lateral gene transfers of both PFO and [FeFe]-H2ase in eubacteria, (ii) decreased support for the monophyly of eukaryote PFO domains, and, (iii) that eukaryotic [FeFe]-H2ases are not monophyletic. Although there are few eukaryote [FeFe]-H2ase maturase orthologs characterized, phylogenies of these proteins do recover eukaryote monophyly, although a consistent eubacterial sister group for eukaryotic homologs could not be determined. An exhaustive search for these five genes in diverse genomes from two representative eubacterial groups, the Clostridiales and the 
-Proteobacteria, shows that while these enzymes are nearly universally present within the former group, they are very rare in the latter. No -proteobacterial genome sequenced to date encodes all five proteins. Molecular phylogenies and the extremely restricted distribution of PFO, [FeFe]-H2ases and their associated maturases within the -Proteobacteria do not support a mitochondrial origin for these enzymes in eukaryotes. However, the unexpected prevalence of PFO, pyruvate:NADP oxidoreductase, [FeFe]-H2ase, and the maturase in genomes of diverse eukaryotes indicates these enzymes have an important role in the evolution of microbial eukaryote energy metabolism.
Key Words: pyruvate:ferredoxin oxidoreductase • hydrogenase • origin • anaerobic • protist