title: Phylogenomic evidence for the presence of a flagellum and cbb(3) oxidase in the free-living mitochondrial ancestor.
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 cbb(3)-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.
authors.affiliation: Dipartimento di Patologia Animale, Igiene e Sanità Pubblica Veterinaria, Università degli Studi di Milano, Milano, Italy.
authors.forename: Davide
authors.initials: D
authors.lastname: Sassera
authors.forename: Nathan
authors.initials: N
authors.lastname: Lo
authors.forename: Sara
authors.initials: S
authors.lastname: Epis
authors.forename: Giuseppe
authors.initials: G
authors.lastname: D'Auria
authors.forename: Matteo
authors.initials: M
authors.lastname: Montagna
authors.forename: Francesco
authors.initials: F
authors.lastname: Comandatore
authors.forename: David
authors.initials: D
authors.lastname: Horner
authors.forename: Juli
authors.initials: J
authors.lastname: Peretó
authors.forename: Alberto Maria
authors.initials: AM
authors.lastname: Luciano
authors.forename: Federica
authors.initials: F
authors.lastname: Franciosi
authors.forename: Emanuele
authors.initials: E
authors.lastname: Ferri
authors.forename: Elena
authors.initials: E
authors.lastname: Crotti
authors.forename: Chiara
authors.initials: C
authors.lastname: Bazzocchi
authors.forename: Daniele
authors.initials: D
authors.lastname: Daffonchio
authors.forename: Luciano
authors.initials: L
authors.lastname: Sacchi
authors.forename: Andres
authors.initials: A
authors.lastname: Moya
authors.forename: Amparo
authors.initials: A
authors.lastname: Latorre
authors.forename: Claudio
authors.initials: C
authors.lastname: Bandi
mesh_terms: D001483:Base Sequence; D005075:Biological Evolution; D003576:Electron Transport Complex IV / Q000235:genetics*; D005057:Eukaryotic Cells; D019143:Evolution, Molecular; D005407:Flagella / Q000235:genetics*; D016680:Genome, Bacterial; D008928:Mitochondria / Q000235:genetics* / Q000502:physiology* / Q000648:ultrastructure*; D010085:Oxidative Phosphorylation; D010802:Phylogeny; D016996:Rickettsieae / Q000235:genetics*; D017422:Sequence Analysis, DNA; D013559:Symbiosis / Q000235:genetics
chemical_list: C414443:cbb3 oxidase; D003576:Electron Transport Complex IV