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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Jan 29;358(1429):165–179. doi: 10.1098/rstb.2002.1193

On the origin of mitochondria: a genomics perspective.

Siv G E Andersson 1, Olof Karlberg 1, Björn Canbäck 1, Charles G Kurland 1
PMCID: PMC1693097  PMID: 12594925

Abstract

The availability of complete genome sequence data from both bacteria and eukaryotes provides information about the contribution of bacterial genes to the origin and evolution of mitochondria. Phylogenetic analyses based on genes located in the mitochondrial genome indicate that these genes originated from within the alpha-proteobacteria. A number of ancestral bacterial genes have also been transferred from the mitochondrial to the nuclear genome, as evidenced by the presence of orthologous genes in the mitochondrial genome in some species and in the nuclear genome of other species. However, a multitude of mitochondrial proteins encoded in the nucleus display no homology to bacterial proteins, indicating that these originated within the eukaryotic cell subsequent to the acquisition of the endosymbiont. An analysis of the expression patterns of yeast nuclear genes coding for mitochondrial proteins has shown that genes predicted to be of eukaryotic origin are mainly translated on polysomes that are free in the cytosol whereas those of putative bacterial origin are translated on polysomes attached to the mitochondrion. The strong relationship with alpha-proteobacterial genes observed for some mitochondrial genes, combined with the lack of such a relationship for others, indicates that the modern mitochondrial proteome is the product of both reductive and expansive processes.

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Selected References

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  1. Akhmanova A., Voncken F., van Alen T., van Hoek A., Boxma B., Vogels G., Veenhuis M., Hackstein J. H. A hydrogenosome with a genome. Nature. 1998 Dec 10;396(6711):527–528. doi: 10.1038/25023. [DOI] [PubMed] [Google Scholar]
  2. Allen J. F. Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol. 1993 Dec 21;165(4):609–631. doi: 10.1006/jtbi.1993.1210. [DOI] [PubMed] [Google Scholar]
  3. Allen J. F., Raven J. A. Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. J Mol Evol. 1996 May;42(5):482–492. doi: 10.1007/BF02352278. [DOI] [PubMed] [Google Scholar]
  4. Andersson J. O., Andersson S. G. Genome degradation is an ongoing process in Rickettsia. Mol Biol Evol. 1999 Sep;16(9):1178–1191. doi: 10.1093/oxfordjournals.molbev.a026208. [DOI] [PubMed] [Google Scholar]
  5. Andersson J. O., Andersson S. G. Insights into the evolutionary process of genome degradation. Curr Opin Genet Dev. 1999 Dec;9(6):664–671. doi: 10.1016/s0959-437x(99)00024-6. [DOI] [PubMed] [Google Scholar]
  6. Andersson J. O., Andersson S. G. Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes. Mol Biol Evol. 2001 May;18(5):829–839. doi: 10.1093/oxfordjournals.molbev.a003864. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Andersson S. G., Kurland C. G. Origins of mitochondria and hydrogenosomes. Curr Opin Microbiol. 1999 Oct;2(5):535–541. doi: 10.1016/s1369-5274(99)00013-2. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Baker K. P., Schatz G. Mitochondrial proteins essential for viability mediate protein import into yeast mitochondria. Nature. 1991 Jan 17;349(6306):205–208. doi: 10.1038/349205a0. [DOI] [PubMed] [Google Scholar]
  12. Baughn Anthony D., Malamy Michael H. A mitochondrial-like aconitase in the bacterium Bacteroides fragilis: implications for the evolution of the mitochondrial Krebs cycle. Proc Natl Acad Sci U S A. 2002 Mar 5;99(7):4662–4667. doi: 10.1073/pnas.052710199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Berg O. G., Kurland C. G. Why mitochondrial genes are most often found in nuclei. Mol Biol Evol. 2000 Jun;17(6):951–961. doi: 10.1093/oxfordjournals.molbev.a026376. [DOI] [PubMed] [Google Scholar]
  14. Bui E. T., Bradley P. J., Johnson P. J. A common evolutionary origin for mitochondria and hydrogenosomes. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9651–9656. doi: 10.1073/pnas.93.18.9651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Canback B., Andersson S. G. E., Kurland C. G. The global phylogeny of glycolytic enzymes. Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6097–6102. doi: 10.1073/pnas.082112499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Clark C. G., Roger A. J. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6518–6521. doi: 10.1073/pnas.92.14.6518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Covello P. S., Gray M. W. Silent mitochondrial and active nuclear genes for subunit 2 of cytochrome c oxidase (cox2) in soybean: evidence for RNA-mediated gene transfer. EMBO J. 1992 Nov;11(11):3815–3820. doi: 10.1002/j.1460-2075.1992.tb05473.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. DelVecchio Vito G., Kapatral Vinayak, Redkar Rajendra J., Patra Guy, Mujer Cesar, Los Tamara, Ivanova Natalia, Anderson Iain, Bhattacharyya Anamitra, Lykidis Athanasios. The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc Natl Acad Sci U S A. 2001 Dec 26;99(1):443–448. doi: 10.1073/pnas.221575398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Embley T. M., Finlay B. J., Dyal P. L., Hirt R. P., Wilkinson M., Williams A. G. Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc Biol Sci. 1995 Oct 23;262(1363):87–93. doi: 10.1098/rspb.1995.0180. [DOI] [PubMed] [Google Scholar]
  20. Embley T. M., Hirt R. P. Early branching eukaryotes? Curr Opin Genet Dev. 1998 Dec;8(6):624–629. doi: 10.1016/s0959-437x(98)80029-4. [DOI] [PubMed] [Google Scholar]
  21. Foury F., Roganti T., Lecrenier N., Purnelle B. The complete sequence of the mitochondrial genome of Saccharomyces cerevisiae. FEBS Lett. 1998 Dec 4;440(3):325–331. doi: 10.1016/s0014-5793(98)01467-7. [DOI] [PubMed] [Google Scholar]
  22. Fraser C. M., Gocayne J. D., White O., Adams M. D., Clayton R. A., Fleischmann R. D., Bult C. J., Kerlavage A. R., Sutton G., Kelley J. M. The minimal gene complement of Mycoplasma genitalium. Science. 1995 Oct 20;270(5235):397–403. doi: 10.1126/science.270.5235.397. [DOI] [PubMed] [Google Scholar]
  23. Galibert F., Finan T. M., Long S. R., Puhler A., Abola P., Ampe F., Barloy-Hubler F., Barnett M. J., Becker A., Boistard P. The composite genome of the legume symbiont Sinorhizobium meliloti. Science. 2001 Jul 27;293(5530):668–672. doi: 10.1126/science.1060966. [DOI] [PubMed] [Google Scholar]
  24. Germot A., Philippe H., Le Guyader H. Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol Biochem Parasitol. 1997 Aug;87(2):159–168. doi: 10.1016/s0166-6851(97)00064-9. [DOI] [PubMed] [Google Scholar]
  25. Goodner B., Hinkle G., Gattung S., Miller N., Blanchard M., Qurollo B., Goldman B. S., Cao Y., Askenazi M., Halling C. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science. 2001 Dec 14;294(5550):2323–2328. doi: 10.1126/science.1066803. [DOI] [PubMed] [Google Scholar]
  26. Gray M. W., Burger G., Lang B. F. Mitochondrial evolution. Science. 1999 Mar 5;283(5407):1476–1481. doi: 10.1126/science.283.5407.1476. [DOI] [PubMed] [Google Scholar]
  27. Gray M. W., Cedergren R., Abel Y., Sankoff D. On the evolutionary origin of the plant mitochondrion and its genome. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2267–2271. doi: 10.1073/pnas.86.7.2267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gray M. W., Lang B. F., Cedergren R., Golding G. B., Lemieux C., Sankoff D., Turmel M., Brossard N., Delage E., Littlejohn T. G. Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res. 1998 Feb 15;26(4):865–878. doi: 10.1093/nar/26.4.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gray M. W. Rickettsia, typhus and the mitochondrial connection. Nature. 1998 Nov 12;396(6707):109–110. doi: 10.1038/24030. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Hackstein J. H., Akhmanova A., Boxma B., Harhangi H. R., Voncken F. G. Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol. 1999 Nov;7(11):441–447. doi: 10.1016/s0966-842x(99)01613-3. [DOI] [PubMed] [Google Scholar]
  32. Hanson R. S., Hanson T. E. Methanotrophic bacteria. Microbiol Rev. 1996 Jun;60(2):439–471. doi: 10.1128/mr.60.2.439-471.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hatch T. P., Al-Hossainy E., Silverman J. A. Adenine nucleotide and lysine transport in Chlamydia psittaci. J Bacteriol. 1982 May;150(2):662–670. doi: 10.1128/jb.150.2.662-670.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Heldt H. W. Adenine nucleotide translocation in spinach chloroplasts. FEBS Lett. 1969 Sep;5(1):11–14. doi: 10.1016/0014-5793(69)80280-2. [DOI] [PubMed] [Google Scholar]
  35. Hirt R. P., Healy B., Vossbrinck C. R., Canning E. U., Embley T. M. A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr Biol. 1997 Dec 1;7(12):995–998. doi: 10.1016/s0960-9822(06)00420-9. [DOI] [PubMed] [Google Scholar]
  36. Hirt R. P., Logsdon J. M., Jr, Healy B., Dorey M. W., Doolittle W. F., Embley T. M. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):580–585. doi: 10.1073/pnas.96.2.580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hodges P. E., McKee A. H., Davis B. P., Payne W. E., Garrels J. I. The Yeast Proteome Database (YPD): a model for the organization and presentation of genome-wide functional data. Nucleic Acids Res. 1999 Jan 1;27(1):69–73. doi: 10.1093/nar/27.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Kalman S., Mitchell W., Marathe R., Lammel C., Fan J., Hyman R. W., Olinger L., Grimwood J., Davis R. W., Stephens R. S. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat Genet. 1999 Apr;21(4):385–389. doi: 10.1038/7716. [DOI] [PubMed] [Google Scholar]
  40. Kampfenkel K., Möhlmann T., Batz O., Van Montagu M., Inzé D., Neuhaus H. E. Molecular characterization of an Arabidopsis thaliana cDNA encoding a novel putative adenylate translocator of higher plants. FEBS Lett. 1995 Nov 6;374(3):351–355. doi: 10.1016/0014-5793(95)01143-3. [DOI] [PubMed] [Google Scholar]
  41. Karlberg O., Canbäck B., Kurland C. G., Andersson S. G. The dual origin of the yeast mitochondrial proteome. Yeast. 2000 Sep 30;17(3):170–187. doi: 10.1002/1097-0061(20000930)17:3<170::AID-YEA25>3.0.CO;2-V. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Katinka M. D., Duprat S., Cornillot E., Méténier G., Thomarat F., Prensier G., Barbe V., Peyretaillade E., Brottier P., Wincker P. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature. 2001 Nov 22;414(6862):450–453. doi: 10.1038/35106579. [DOI] [PubMed] [Google Scholar]
  43. Kita Kiyoshi, Hirawake Hiroko, Miyadera Hiroko, Amino Hisako, Takeo Satoru. Role of complex II in anaerobic respiration of the parasite mitochondria from Ascaris suum and Plasmodium falciparum. Biochim Biophys Acta. 2002 Jan 17;1553(1-2):123–139. doi: 10.1016/s0005-2728(01)00237-7. [DOI] [PubMed] [Google Scholar]
  44. Koehler C. M. Protein translocation pathways of the mitochondrion. FEBS Lett. 2000 Jun 30;476(1-2):27–31. doi: 10.1016/s0014-5793(00)01664-1. [DOI] [PubMed] [Google Scholar]
  45. Kuan J., Saier M. H., Jr The mitochondrial carrier family of transport proteins: structural, functional, and evolutionary relationships. Crit Rev Biochem Mol Biol. 1993;28(3):209–233. doi: 10.3109/10409239309086795. [DOI] [PubMed] [Google Scholar]
  46. Kurland C. G., Andersson S. G. Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev. 2000 Dec;64(4):786–820. doi: 10.1128/mmbr.64.4.786-820.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Lin Su-Ju, Kaeberlein Matt, Andalis Alex A., Sturtz Lori A., Defossez Pierre-Antoine, Culotta Valeria C., Fink Gerald R., Guarente Leonard. Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature. 2002 Jul 18;418(6895):344–348. doi: 10.1038/nature00829. [DOI] [PubMed] [Google Scholar]
  49. Marc Philippe, Margeot Antoine, Devaux Frederic, Blugeon Corinne, Corral-Debrinski Marisol, Jacq Claude. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 2002 Jan 29;3(2):159–164. doi: 10.1093/embo-reports/kvf025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Martin W., Müller M. The hydrogen hypothesis for the first eukaryote. Nature. 1998 Mar 5;392(6671):37–41. doi: 10.1038/32096. [DOI] [PubMed] [Google Scholar]
  51. Moreira D, Lopez-Garcia P. Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis . J Mol Evol. 1998 Nov;47(5):517–530. doi: 10.1007/pl00006408. [DOI] [PubMed] [Google Scholar]
  52. Möhlmann T., Tjaden J., Schwöppe C., Winkler H. H., Kampfenkel K., Neuhaus H. E. Occurrence of two plastidic ATP/ADP transporters in Arabidopsis thaliana L.--molecular characterisation and comparative structural analysis of similar ATP/ADP translocators from plastids and Rickettsia prowazekii. Eur J Biochem. 1998 Mar 15;252(3):353–359. doi: 10.1046/j.1432-1327.1998.2520353.x. [DOI] [PubMed] [Google Scholar]
  53. Müller M. The hydrogenosome. J Gen Microbiol. 1993 Dec;139(12):2879–2889. doi: 10.1099/00221287-139-12-2879. [DOI] [PubMed] [Google Scholar]
  54. Neuhaus H. E., Henrichs G., Scheibe R. Characterization of Glucose-6-Phosphate Incorporation into Starch by Isolated Intact Cauliflower-Bud Plastids. Plant Physiol. 1993 Feb;101(2):573–578. doi: 10.1104/pp.101.2.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Nierman W. C., Feldblyum T. V., Laub M. T., Paulsen I. T., Nelson K. E., Eisen J. A., Heidelberg J. F., Alley M. R., Ohta N., Maddock J. R. Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci U S A. 2001 Mar 20;98(7):4136–4141. doi: 10.1073/pnas.061029298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Nugent J. M., Palmer J. D. RNA-mediated transfer of the gene coxII from the mitochondrion to the nucleus during flowering plant evolution. Cell. 1991 Aug 9;66(3):473–481. doi: 10.1016/0092-8674(81)90011-8. [DOI] [PubMed] [Google Scholar]
  57. Ogata H., Audic S., Renesto-Audiffren P., Fournier P. E., Barbe V., Samson D., Roux V., Cossart P., Weissenbach J., Claverie J. M. Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science. 2001 Sep 14;293(5537):2093–2098. doi: 10.1126/science.1061471. [DOI] [PubMed] [Google Scholar]
  58. Olsen G. J., Woese C. R., Overbeek R. The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol. 1994 Jan;176(1):1–6. doi: 10.1128/jb.176.1.1-6.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Peyretaillade E., Biderre C., Peyret P., Duffieux F., Méténier G., Gouy M., Michot B., Vivarès C. P. Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res. 1998 Aug 1;26(15):3513–3520. doi: 10.1093/nar/26.15.3513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Peyretaillade E., Broussolle V., Peyret P., Méténier G., Gouy M., Vivarès C. P. Microsporidia, amitochondrial protists, possess a 70-kDa heat shock protein gene of mitochondrial evolutionary origin. Mol Biol Evol. 1998 Jun;15(6):683–689. doi: 10.1093/oxfordjournals.molbev.a025971. [DOI] [PubMed] [Google Scholar]
  61. Pfeiffer T., Schuster S., Bonhoeffer S. Cooperation and competition in the evolution of ATP-producing pathways. Science. 2001 Mar 29;292(5516):504–507. doi: 10.1126/science.1058079. [DOI] [PubMed] [Google Scholar]
  62. Pozueta-Romero J., Frehner M., Viale A. M., Akazawa T. Direct transport of ADPglucose by an adenylate translocator is linked to starch biosynthesis in amyloplasts. Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5769–5773. doi: 10.1073/pnas.88.13.5769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Pronk J. T., Yde Steensma H., Van Dijken J. P. Pyruvate metabolism in Saccharomyces cerevisiae. Yeast. 1996 Dec;12(16):1607–1633. doi: 10.1002/(sici)1097-0061(199612)12:16<1607::aid-yea70>3.0.co;2-4. [DOI] [PubMed] [Google Scholar]
  64. Roger A. J., Svärd S. G., Tovar J., Clark C. G., Smith M. W., Gillin F. D., Sogin M. L. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):229–234. doi: 10.1073/pnas.95.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Rotte C., Henze K., Müller M., Martin W. Origins of hydrogenosomes and mitochondria. Curr Opin Microbiol. 2000 Oct;3(5):481–486. doi: 10.1016/s1369-5274(00)00126-0. [DOI] [PubMed] [Google Scholar]
  66. Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 1996 Mar 15;271(5255):1519–1526. doi: 10.1126/science.271.5255.1519. [DOI] [PubMed] [Google Scholar]
  67. Schunemann D., Borchert S., Flugge U. I., Heldt H. W. ADP/ATP Translocator from Pea Root Plastids (Comparison with Translocators from Spinach Chloroplasts and Pea Leaf Mitochondria). Plant Physiol. 1993 Sep;103(1):131–137. doi: 10.1104/pp.103.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. 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]
  69. Stephens R. S., Kalman S., Lammel C., Fan J., Marathe R., Aravind L., Mitchell W., Olinger L., Tatusov R. L., Zhao Q. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science. 1998 Oct 23;282(5389):754–759. doi: 10.1126/science.282.5389.754. [DOI] [PubMed] [Google Scholar]
  70. Stucki J. W. The optimal efficiency and the economic degrees of coupling of oxidative phosphorylation. Eur J Biochem. 1980 Aug;109(1):269–283. doi: 10.1111/j.1432-1033.1980.tb04792.x. [DOI] [PubMed] [Google Scholar]
  71. Takaya N., Suzuki S., Kuwazaki S., Shoun H., Maruo F., Yamaguchi M., Takeo K. Cytochrome p450nor, a novel class of mitochondrial cytochrome P450 involved in nitrate respiration in the fungus Fusarium oxysporum. Arch Biochem Biophys. 1999 Dec 15;372(2):340–346. doi: 10.1006/abbi.1999.1499. [DOI] [PubMed] [Google Scholar]
  72. Thorsness P. E., Fox T. D. Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature. 1990 Jul 26;346(6282):376–379. doi: 10.1038/346376a0. [DOI] [PubMed] [Google Scholar]
  73. Thorsness P. E., Fox T. D. Nuclear mutations in Saccharomyces cerevisiae that affect the escape of DNA from mitochondria to the nucleus. Genetics. 1993 May;134(1):21–28. doi: 10.1093/genetics/134.1.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Tielens A. G. Energy generation in parasitic helminths. Parasitol Today. 1994 Sep;10(9):346–352. doi: 10.1016/0169-4758(94)90245-3. [DOI] [PubMed] [Google Scholar]
  75. Tielens A. G., Van Hellemond J. J. The electron transport chain in anaerobically functioning eukaryotes. Biochim Biophys Acta. 1998 Jun 10;1365(1-2):71–78. doi: 10.1016/s0005-2728(98)00045-0. [DOI] [PubMed] [Google Scholar]
  76. Tielens Aloysius G. M., Rotte Carmen, van Hellemond Jaap J., Martin William. Mitochondria as we don't know them. Trends Biochem Sci. 2002 Nov;27(11):564–572. doi: 10.1016/s0968-0004(02)02193-x. [DOI] [PubMed] [Google Scholar]
  77. Unseld M., Marienfeld J. R., Brandt P., Brennicke A. The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997 Jan;15(1):57–61. doi: 10.1038/ng0197-57. [DOI] [PubMed] [Google Scholar]
  78. Van Hellemond J. J., Tielens A. G. Expression and functional properties of fumarate reductase. Biochem J. 1994 Dec 1;304(Pt 2):321–331. doi: 10.1042/bj3040321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. 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]
  80. Voncken Frank, Boxma Brigitte, Tjaden Joachim, Akhmanova Anna, Huynen Martijn, Verbeek Fons, Tielens Aloysius G. M., Haferkamp Ilka, Neuhaus H. Ekkehard, Vogels Godfried. Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp. Mol Microbiol. 2002 Jun;44(6):1441–1454. doi: 10.1046/j.1365-2958.2002.02959.x. [DOI] [PubMed] [Google Scholar]
  81. Walker J. E., Runswick M. J. The mitochondrial transport protein superfamily. J Bioenerg Biomembr. 1993 Oct;25(5):435–446. doi: 10.1007/BF01108401. [DOI] [PubMed] [Google Scholar]
  82. Wheeler D. L., Chappey C., Lash A. E., Leipe D. D., Madden T. L., Schuler G. D., Tatusova T. A., Rapp B. A. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2000 Jan 1;28(1):10–14. doi: 10.1093/nar/28.1.10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Williamson L. R., Plano G. V., Winkler H. H., Krause D. C., Wood D. O. Nucleotide sequence of the Rickettsia prowazekii ATP/ADP translocase-encoding gene. Gene. 1989 Aug 15;80(2):269–278. doi: 10.1016/0378-1119(89)90291-6. [DOI] [PubMed] [Google Scholar]
  84. Winkler H. H. Rickettsial permeability. An ADP-ATP transport system. J Biol Chem. 1976 Jan 25;251(2):389–396. [PubMed] [Google Scholar]
  85. 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]
  86. Wood D. W., Setubal J. C., Kaul R., Monks D. E., Kitajima J. P., Okura V. K., Zhou Y., Chen L., Wood G. E., Almeida N. F., Jr The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science. 2001 Dec 14;294(5550):2317–2323. doi: 10.1126/science.1066804. [DOI] [PubMed] [Google Scholar]
  87. Yang D., Oyaizu Y., Oyaizu H., Olsen G. J., Woese C. R. Mitochondrial origins. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4443–4447. doi: 10.1073/pnas.82.13.4443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Zumft W. G. Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev. 1997 Dec;61(4):533–616. doi: 10.1128/mmbr.61.4.533-616.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. van Hoek A. H., Akhmanova A. S., Huynen M. A., Hackstein J. H. A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol Biol Evol. 2000 Jan;17(1):202–206. doi: 10.1093/oxfordjournals.molbev.a026234. [DOI] [PubMed] [Google Scholar]
  90. van der Giezen M., Rechinger K. B., Svendsen I., Durand R., Hirt R. P., Fèvre M., Embley T. M., Prins R. A. A mitochondrial-like targeting signal on the hydrogenosomal malic enzyme from the anaerobic fungus Neocallimastix frontalis: support for the hypothesis that hydrogenosomes are modified mitochondria. Mol Microbiol. 1997 Jan;23(1):11–21. doi: 10.1046/j.1365-2958.1997.1891553.x. [DOI] [PubMed] [Google Scholar]
  91. van der Giezen M., Sjollema K. A., Artz R. R., Alkema W., Prins R. A. Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS Lett. 1997 May 19;408(2):147–150. doi: 10.1016/s0014-5793(97)00409-2. [DOI] [PubMed] [Google Scholar]
  92. van der Giezen Mark, Slotboom Dirk Jan, Horner David S., Dyal Patricia L., Harding Marilyn, Xue Gang-Ping, Embley T. Martin, Kunji Edmund R. S. Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. EMBO J. 2002 Feb 15;21(4):572–579. doi: 10.1093/emboj/21.4.572. [DOI] [PMC free article] [PubMed] [Google Scholar]

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