Phylogenomic evidence for the presence of a flagellum and cbb 3 oxidase in the free-living mitochondrial ancestor

Davide Sassera, Nathan Lo, Sara Epis, Giuseppe D'Auria, Matteo Montagna, Francesco Comandatore, David Horner, Juli Peretó, Alberto Maria Luciano, Federica Franciosi, Emanuele Ferri, Elena Crotti, Chiara Bazzocchi, Daniele Daffonchio, Luciano Sacchi, Andres Moya, Amparo Latorre, Claudio Bandi*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

77 Scopus citations

Abstract

The initiation of the intracellular symbiosis that would give rise to mitochondria and eukaryotes was a major event in the history of life on earth. Hypotheses to explain eukaryogenesis fall into two broad and competing categories: those proposing that the host was a phagocytotic proto-eukaryote that preyed upon the free-living mitochondrial ancestor (hereafter FMA), and those proposing that the host was an archaebacterium that engaged in syntrophy with the FMA. Of key importance to these hypotheses are whether the FMA was motile or nonmotile, and the atmospheric conditions under which the FMA thrived. Reconstructions of the FMA based on genome content of Rickettsiales representatives-generally considered to be the closest living relatives of mitochondria-indicate that it was nonmotile and aerobic. We have sequenced the genome of Candidatus Midichloria mitochondrii, a novel and phylogenetically divergent member of the Rickettsiales. We found that it possesses unique gene sets found in no other Rickettsiales, including 26 genes associated with flagellar assembly, and a cbb3-type cytochrome oxidase. Phylogenomic analyses show that these genes were inherited in a vertical fashion from an ancestral α-proteobacterium, and indicate that the FMA possessed a flagellum, and could undergo oxidative phosphorylation under both aerobic and microoxic conditions. These results indicate that the FMA played a more active and potentially parasitic role in eukaryogenesis than currently appreciated and provide an explanation for how the symbiosis could have evolved under low levels of oxygen.

Original languageEnglish (US)
Pages (from-to)3285-3296
Number of pages12
JournalMolecular biology and evolution
Volume28
Issue number12
DOIs
StatePublished - Dec 1 2011

Keywords

  • Midichloria mitochondrii
  • eukaryogenesis
  • mitochondrion
  • phylogenomics
  • rickettsiales
  • symbiosis

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

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