Iron hydrogenases and the evolution of anaerobic eukaryotes

Mol Biol Evol. 2000 Nov;17(11):1695-709. doi: 10.1093/oxfordjournals.molbev.a026268.


Hydrogenases, oxygen-sensitive enzymes that can make hydrogen gas, are key to the function of hydrogen-producing organelles (hydrogenosomes), which occur in anaerobic protozoa scattered throughout the eukaryotic tree. Hydrogenases also play a central role in the hydrogen and syntrophic hypotheses for eukaryogenesis. Here, we show that sequences related to iron-only hydrogenases ([Fe] hydrogenases) are more widely distributed among eukaryotes than reports of hydrogen production have suggested. Genes encoding small proteins which contain conserved structural features unique to [Fe] hydrogenases were identified on all well-surveyed aerobic eukaryote genomes. Longer sequences encoding [Fe] hydrogenases also occur in the anaerobic eukaryotes Entamoeba histolytica and Spironucleus barkhanus, both of which lack hydrogenosomes. We also identified a new [Fe] hydrogenase sequence from Trichomonas vaginalis, bringing the total of [Fe] hydrogenases reported for this organism to three, all of which may function within its hydrogenosomes. Phylogenetic analysis and hypothesis testing using likelihood ratio tests and parametric bootstrapping suggest that the [Fe] hydrogenases in anaerobic eukaryotes are not monophyletic. Iron-only hydrogenases from Entamoeba, Spironucleus, and Trichomonas are plausibly monophyletic, consistent with the hypothesis that a gene for [Fe] hydrogenase was already present on the genome of the common, perhaps also anaerobic, ancestor of these phylogenetically distinct eukaryotes. Trees where the [Fe] hydrogenase from the hydrogenosomal ciliate Nyctotherus was constrained to be monophyletic with the other eukaryote sequences were rejected using a likelihood ratio test of monophyly. In most analyses, the Nyctotherus sequence formed a sister group with a [Fe] hydrogenase on the genome of the eubacterium Desulfovibrio vulgaris. Thus, it is possible that Nyctotherus obtained its hydrogenosomal [Fe] hydrogenase from a different source from Trichomonas for its hydrogenosomes. We find no support for the hypothesis that components of the Nyctotherus [Fe] hydrogenase fusion protein derive from the mitochondrial respiratory chain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Anaerobiosis
  • Animals
  • Cytosol / enzymology
  • DNA, Complementary / chemistry
  • DNA, Complementary / genetics
  • DNA, Protozoan / chemistry
  • DNA, Protozoan / genetics
  • Diplomonadida / enzymology
  • Diplomonadida / genetics
  • Entamoeba histolytica / enzymology
  • Entamoeba histolytica / genetics
  • Eukaryota / enzymology
  • Eukaryota / genetics*
  • Eukaryotic Cells / enzymology
  • Evolution, Molecular*
  • Hydrogenase / genetics*
  • Iron-Sulfur Proteins / genetics*
  • Molecular Sequence Data
  • Phylogeny
  • Sequence Alignment
  • Sequence Analysis, DNA
  • Sequence Homology, Amino Acid
  • Trichomonas vaginalis / enzymology
  • Trichomonas vaginalis / genetics


  • DNA, Complementary
  • DNA, Protozoan
  • Iron-Sulfur Proteins
  • iron hydrogenase
  • Hydrogenase

Associated data

  • GENBANK/AF262400
  • GENBANK/AF262401
  • GENBANK/AF262402