Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss

William H. Lewis, Anders E. Lind, Kacper M. Sendra, Henning Onsbring, Tom A. Williams, Genoveva F. Esteban, Robert P. Hirt, Thijs J.G. Ettema, T.M. Embley

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Abstract

Hydrogenosomes are H2-producing mitochondrial homologs found in some anaerobic microbial eukaryotes that provide a rare intracellular niche for H2-utilizing endosymbiotic archaea. Among ciliates, anaerobic and aerobic lineages are interspersed, demonstrating that the switch to an anaerobic lifestyle with hydrogenosomes has occurred repeatedly and independently. To investigate the molecular details of this transition, we generated genomic and transcriptomic data sets from anaerobic ciliates representing three distinct lineages. Our data demonstrate that hydrogenosomes have evolved from ancestral mitochondria in each case and reveal different degrees of independent mitochondrial genome and proteome reductive evolution, including the first example of complete mitochondrial genome loss in ciliates. Intriguingly, the FeFe-hydrogenase used for generating H2 has a unique domain structure among eukaryotes and appears to have been present, potentially through a single lateral gene transfer from an unknown donor, in the common aerobic ancestor of all three lineages. The early acquisition and retention of FeFe-hydrogenase helps to explain the facility whereby mitochondrial function can be so radically modified within this diverse and ecologically important group of microbial eukaryotes.

Original languageEnglish
Pages (from-to)524-539
JournalMolecular Biology and Evolution
Volume37
Issue number2
DOIs
Publication statusPublished - Feb 2020

Keywords

  • anaerobic metabolism
  • evolution
  • genomics
  • hydrogenosomes
  • microbial eukaryotes
  • mitochondria

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    Lewis, W. H., Lind, A. E., Sendra, K. M., Onsbring, H., Williams, T. A., Esteban, G. F., Hirt, R. P., Ettema, T. J. G., & Embley, T. M. (2020). Convergent Evolution of Hydrogenosomes from Mitochondria by Gene Transfer and Loss. Molecular Biology and Evolution, 37(2), 524-539. https://doi.org/10.1093/molbev/msz239