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The Dual Origin of the Yeast Mitochondrial Proteome

Olof Karlberg 1, Björn Canbäck 1, Charles G Kurland 1, Siv G E Andersson 1,2,✉
PMCID: PMC2448374  PMID: 11025528

Abstract

We propose a scheme for the origin of mitochondria based on phylogenetic reconstructions with more than 400 yeast nuclear genes that encode mitochondrial proteins. Half of the yeast mitochondrial proteins have no discernable bacterial homologues, while one-tenth are unequivocally of α-proteobacterial origin. These data suggest that the majority of genes encoding yeast mitochondrial proteins are descendants of two different genomic lineages that have evolved in different modes. First, the ancestral free-living α-proteobacterium evolved into an endosymbiont of an anaerobic host. Most of the ancestral bacterial genes were lost, but a small fraction of genes supporting bioenergetic and translational processes were retained and eventually transferred to what became the host nuclear genome. In a second, parallel mode, a larger number of novel mitochondrial genes were recruited from the nuclear genome to complement the remaining genes from the bacterial ancestor. These eukaryotic genes, which are primarily involved in transport and regulatory functions, transformed the endosymbiont into an ATP-exporting organelle.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andersson S. G. Bioenergetics of the obligate intracellular parasite Rickettsia prowazekii. Biochim Biophys Acta. 1998 Jun 10;1365(1-2):105–111. doi: 10.1016/s0005-2728(98)00050-4. [DOI] [PubMed] [Google Scholar]
  3. Andersson S. G., Kurland C. G. Reductive evolution of resident genomes. Trends Microbiol. 1998 Jul;6(7):263–268. doi: 10.1016/s0966-842x(98)01312-2. [DOI] [PubMed] [Google Scholar]
  4. Andersson S. G., Zomorodipour A., Andersson J. O., Sicheritz-Pontén T., Alsmark U. C., Podowski R. M., Näslund A. K., Eriksson A. S., Winkler H. H., Kurland C. G. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature. 1998 Nov 12;396(6707):133–140. doi: 10.1038/24094. [DOI] [PubMed] [Google Scholar]
  5. Burger G., Lang B. F., Reith M., Gray M. W. Genes encoding the same three subunits of respiratory complex II are present in the mitochondrial DNA of two phylogenetically distant eukaryotes. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2328–2332. doi: 10.1073/pnas.93.6.2328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gray M. W. The endosymbiont hypothesis revisited. Int Rev Cytol. 1992;141:233–357. doi: 10.1016/s0074-7696(08)62068-9. [DOI] [PubMed] [Google Scholar]
  7. Horner D. S., Hirt R. P., Embley T. M. A single eubacterial origin of eukaryotic pyruvate: ferredoxin oxidoreductase genes: implications for the evolution of anaerobic eukaryotes. Mol Biol Evol. 1999 Sep;16(9):1280–1291. doi: 10.1093/oxfordjournals.molbev.a026218. [DOI] [PubMed] [Google Scholar]
  8. Lang B. F., Burger G., O'Kelly C. J., Cedergren R., Golding G. B., Lemieux C., Sankoff D., Turmel M., Gray M. W. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature. 1997 May 29;387(6632):493–497. doi: 10.1038/387493a0. [DOI] [PubMed] [Google Scholar]
  9. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  10. Sicheritz-Pontén T., Kurland C. G., Andersson S. G. A phylogenetic analysis of the cytochrome b and cytochrome c oxidase I genes supports an origin of mitochondria from within the Rickettsiaceae. Biochim Biophys Acta. 1998 Jul 20;1365(3):545–551. doi: 10.1016/s0005-2728(98)00099-1. [DOI] [PubMed] [Google Scholar]
  11. Viale A. M., Arakaki A. K. The chaperone connection to the origins of the eukaryotic organelles. FEBS Lett. 1994 Mar 21;341(2-3):146–151. doi: 10.1016/0014-5793(94)80446-x. [DOI] [PubMed] [Google Scholar]
  12. Wolf Y. I., Aravind L., Koonin E. V. Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet. 1999 May;15(5):173–175. doi: 10.1016/s0168-9525(99)01704-7. [DOI] [PubMed] [Google Scholar]
  13. Wolfe K. H., Shields D. C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997 Jun 12;387(6634):708–713. doi: 10.1038/42711. [DOI] [PubMed] [Google Scholar]

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