Current Genetics

, Volume 50, Issue 4, pp 225–245 | Cite as

Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering!

  • Johannes H. P. HacksteinEmail author
  • Joachim Tjaden
  • Martijn Huynen
Review Article


One hundred years ago, C. Mereschkowsky, “Privatdozent an der Kaiserlichen Universität in Kasan (Russia)” published a notoriously ignored landmark paper: “Über Natur und Ursprung der Chromatophoren im Pflanzenreiche.” (“On the nature and origin of the chromatophores in the plant kingdom”; Mereschkowsky 1905). In spite of the fact that this paper was written in German (the lingua franca in biology at the time), its fate was similar to Mendel’s publication, which signified, in retrospect, the birth of genetics (Mendel 1865). Both before and after the publication of Mereschkowsky’s article there were many publications dealing with plant “chimera’s” and cytoplasmic inheritance in plants, which should have favoured the interpretation of plastids as “semi-autonomous” symbiotic entities in the cytoplasm of the eukaryotic plant cell (e.g. Braun 1873; Hildebrand 1908; Baur 1909; Renner 1922, 1924, 1934, 1936a, b; Darlington 1929; Stubbe 1959; Tilney-Basset 1963). In addition,...


Mitochondrial Genome Mitochondrial Complex Cluster Biosynthesis Endosymbiotic Origin Mitochondrial Carrier Family 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We gratefully acknowledge the permission to use genome sequence data of Trichomonas provided by The Institute for Genomic Research (TIGR) with funding of the NIH/NIAID. We thank Uwe Maier, Martin Schlegel and Louis Tielens for critical reading, and Alan Schwartz for improving the phrasing.


  1. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V (2004) Complete genome sequence of the Apicomplexan, Cryptosporidium parvum. Science 304:441–445PubMedCrossRefGoogle Scholar
  2. Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Browser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52(5):399–451PubMedCrossRefGoogle Scholar
  3. Akhmanova A, Voncken FG, van Alen A, van Hoek A, Boxma B, Vogels GD, Veenhuis M, Hackstein JHP (1998a) A hydrogenosome with a genome. Nature 396:527–528CrossRefGoogle Scholar
  4. Akhmanova A, Voncken FGJ, Harhangi H, Hosea KM, Vogels GD, Hackstein JHP (1998b) Cytosolic enzymes with a mitochondrial ancestry from the anaerobic chytrid Piromyces sp E2. Mol Microbiol 30:1017–1027CrossRefGoogle Scholar
  5. Akhmanova A, Voncken FGJ, Hosea KM, Harhangi H, Keltjens JT, op den CampHJ, Vogels GD, Hackstein JHP (1999) A hydrogenosome with pyruvate formate-lyase: anaerobic chytrid fungi use an alternative route for pyruvate catabolism. Mol Microbiol 32(5):1103–1114PubMedCrossRefGoogle Scholar
  6. Alon U (2003) Biological networks: the tinkerer as an engineer. Science 301(5641):1866–1867PubMedCrossRefGoogle Scholar
  7. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  8. Amiri H, Karlberg O, Andersson SG (2003) Deep origin of plastid/parasite ATP/ADP translocases. J Mol Evol 56:137–150PubMedCrossRefGoogle Scholar
  9. Andersson SGE, Zomorodipour A, Andersson JO, Sicheritz-Ponten T, Alsmark UC, Podowski RM, Naslund AK, Eriksson AS, Winkler HH, Kurland CG (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133–140PubMedCrossRefGoogle Scholar
  10. Andersson JO, Sjogren AM, Davis LAM, Embley TM, Roger AJ (2003) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13(2):94–104PubMedCrossRefGoogle Scholar
  11. Balk J, Lill R (2004) The cell’s cookbook for iron–sulfur clusters: recipies for fool’s gold? Chem BioChem 5:1044–1049Google Scholar
  12. Baur E (1909) Das Wesen und die Erblichkeitsverhältnisse der varietates albimarginatae hort. von Pelargonium zonale. Z. induct. Abstamm.- u. Vererbungsl 1:330–351CrossRefGoogle Scholar
  13. Benton MJ, Twitchett RJ (2003) How to kill (almost) all life: the end-Permian extinction event. Trends Ecol Evol 18(7):358–365CrossRefGoogle Scholar
  14. Bereiter-Hahn J (1990) Behavior of mitochondria in the living cell. Int Rev Cytol 122:1–63PubMedCrossRefGoogle Scholar
  15. Berry S (2003) Endosymbiosis and the design of eukaryotic electron transport. Biochim Biophys Acta-Bioenerg 1606(1–3):57–72CrossRefGoogle Scholar
  16. Biagini GA, Finlay BJ, Lloyd D (1997) Evolution of the hydrogenosome. FEMS Microbiol Lett 155(2):133–140PubMedCrossRefGoogle Scholar
  17. Bleijlevens B, Buhrke T, van der Linden E, Friedrich B, Albracht SPJ (2004) The auxiliary protein HypX provides oxygen tolerance to the soluble [NiFe]-hydrogenase of Ralstonia eutropha H16 by way of a cyanide ligand to nickel. J Biol Chem 279:46686–46691PubMedCrossRefGoogle Scholar
  18. Boxma B, Voncken F, Jannink S, van Alen T, Akhmanova A, van Weelden SWH, van Hellemond JJ, Ricard G, Huynen M, Tielens AGM, Hackstein JHP (2004) The anaerobic chytridiomycete fungus Piromyces sp E2 produces ethanol via pyruvate:formate lyase and an alcohol dehydrogenase E. Mol Microbiol 51:1389–1399PubMedCrossRefGoogle Scholar
  19. Boxma B, de Graaf RM, van der Staay GWM, van Alen TA, Ricard G, Gabaldon T, van Hoek AHAM, Moon-van der Staay SY, Koopman WJH, van Hellemond JJ, Tielens AGM, Friedrich T, Veenhuis M, Huynen MA, Hackstein JHP (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434:74–79PubMedCrossRefGoogle Scholar
  20. Braun A (1873) Über Cytisus Adami I. Bot Z 31:636–664Google Scholar
  21. Buchner P (1953) Endosymbose der Tiere mit pflanzlichen Mikroorganismen. Birkhäuser basel/stuttgart (English translation: Buchner P 1965). Endosymbiosis of animals with plant microorganisms. Wiley, New YorkGoogle Scholar
  22. Bui ETN, Bradley PJ, Johnson PJ (1996) A common evolutionary origin for the mitochondria and hydrogenosomes. Proc Natl Acad Sci USA 93:9651–9656PubMedCrossRefGoogle Scholar
  23. Bullerwell CE, Lang BF (2005) Fungal evolution: the case of the vanishing mitochondrion. Curr Opin Microbiol 8:362–369PubMedCrossRefGoogle Scholar
  24. Bullerwell CE, Gray MW (2004) The evolution of the mitochondrial genome: protist connections to animals, fungi and plants. Curr Opin Microbiol 7:528–534PubMedCrossRefGoogle Scholar
  25. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716PubMedCrossRefGoogle Scholar
  26. Chan KW, Slotboom DJ, Cox S, Embley TM, Fabre O, van der Giezen M, Harding M, Horner DS, Kunji ERS, Leon-Avila G, Tovar J (2005) A novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr Biol 15:737–742PubMedCrossRefGoogle Scholar
  27. Clark CG, Roger AJ (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci USA 92:6518–6521PubMedCrossRefGoogle Scholar
  28. Clemens DL, Johnson PJ (2000) Failure to detect DNA in hydrogenosomes of Trichomonas vaginalis by nick translation and immunomicroscopy. Mol Biochem Parasit 106:307–313CrossRefGoogle Scholar
  29. Cotter D, Guda P, Fahy E, Subramaniam S (2004) MitoProteome: mitochondrial protein sequence database and annotation system. Nucleic Acids Res 32:D463–D467PubMedCrossRefGoogle Scholar
  30. Darlington CD (1929) Variegation and albinism in Vicia faba. J Genet 21:161CrossRefGoogle Scholar
  31. De Bary A (1878) Ueber Symbiose. Tageblatt der 51. Versammlung deutscher Naturforscher und Aerzte in Cassel 1878. Druck von Baier und Lewalter in Cassel, pp 121–126Google Scholar
  32. De Bary A (1879) Die Erscheinung der Symbiose. Vortrag gehalten auf der versammlung deutscher Naturforscher und Aerzte zu Cassel. Verlag Karl Trübner StrassburgGoogle Scholar
  33. de Duve C (2005) Singulartities: Landmarks on the pathways of life. Cambridge University Press, CambridgeGoogle Scholar
  34. Degli Esposti M (1998) Inhibitors of NADH-ubiquinone reductase: an overview. Biochim Biophys Acta 1364:222–235PubMedCrossRefGoogle Scholar
  35. de Vries DD, de Wijs IJ, Wolff G, Ketelsen UP, Ropers HH, van Oost BA (1993) X-linked myoclonus epilepsy explained as a maternally inherited mitochondrial disorder. Hum Genet 91:51–54PubMedCrossRefGoogle Scholar
  36. del Arco A, Satrustegui J (2005) New mitochondrial carriers: an overview. Cell Mol Life Sci 62:2204–2227PubMedCrossRefGoogle Scholar
  37. Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Am Nat 154(Suppl):S164–S177PubMedCrossRefGoogle Scholar
  38. Delwiche CF (2004) The genomic palimpsest: genomics in evolution and ecology. BioScience 54(11):991–1001CrossRefGoogle Scholar
  39. Douglas AE (1994) Symbiotic interactions. Oxford University Press, OxfordGoogle Scholar
  40. Dyall SD, Johnson PJ (2000) Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr Opin Microbiol 3:404–411PubMedCrossRefGoogle Scholar
  41. Dyall SD, Koehler CM, Delgadillo-Correa MG, Bradley PJ, Plümper E, Leuenberger D, Turck CW, Johnson PJ (2000) Presence of a member of the mitochondrial carrier family in hydrogenosomes: conservation of membrane-targeting pathways between hydrogenosomes and mitochondria. Mol Cell Biol 20:2488–2497PubMedCrossRefGoogle Scholar
  42. Dyall SD, Lester DC, Schneider RE, Delgadillo-Correa MG, Plümper E, Martinez A, Koehler CM, Johnson PJ (2003) Trichomonas vaginalis HMP35, a putative pore-forming hydrogenosomal membrane protein, can form a complex in yeast mitochondria. J Biol Chem 278:30548–30561PubMedCrossRefGoogle Scholar
  43. Dyall SD, Brown MT, Johnson PJ (2004a) Ancient invasions: from endosymbionts to organelles. Science 304:253–257CrossRefGoogle Scholar
  44. Dyall SD, Yan WH, Delgadillo-Correa MG, Lunceford A, Loo JA, Clarke CF, Johnson PJ (2004b) Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431:1103–1107CrossRefGoogle Scholar
  45. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797PubMedCrossRefGoogle Scholar
  46. Embley TM, Finlay BJ, Dyal PL, Hirt RP, Wilkinson M, Williams AG (1995) Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc R Soc Lond B 262:87–93CrossRefGoogle Scholar
  47. Embley TM, Horner DA, Hirt RP (1997) Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria? Trends Ecol Evol 12:437–441CrossRefGoogle Scholar
  48. Embley TM, van der Giezen M, Horner DS, Dyal PL, Bell S, Foster PG (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55:387–95PubMedCrossRefGoogle Scholar
  49. Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630PubMedCrossRefGoogle Scholar
  50. Ernster L, Schatz G (1981) Mitochondria: a historical review. J Cell Biol 91(3):227S–255SPubMedCrossRefGoogle Scholar
  51. Erwin DH (1998) The end and the beginning: recoveries from mass extinctions. Trends Ecol Evol 13(9):344–349CrossRefGoogle Scholar
  52. Esser C, Ahmadinejad N, Wiegand C, Rotte C, Sebastiani F, Gelius-Dietrich G, Henze K, Kretschmann E, Richly E, Leister D, Bryant D, Steel MA, Lockhart PJ, Penny D, Martin W (2004) A genome phylogeny for mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol 21:1643–1660PubMedCrossRefGoogle Scholar
  53. Feagin JE (2000) Mitochondrial genome diversity in parasites. Int J Parasit 30:371–390CrossRefGoogle Scholar
  54. Fenchel T, Finlay BJ (1995) Ecology and evolution in anoxic worlds. Oxford University Press, OxfordGoogle Scholar
  55. Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25:319–324PubMedCrossRefGoogle Scholar
  56. Gabaldon T (2005) Origin and evolution of the mitochondrial proteome. Applications for protein function prediction in the eukaryotes. Thesis Nijmegen 2005. ISBN:90-9019731–1Google Scholar
  57. Gabaldon T, Huynen MA (2003) Reconstruction of the proto-mitochondrial metabolism. Science 301(5633):609–609PubMedCrossRefGoogle Scholar
  58. Gabaldon T, Huynen MA (2004) Shaping the mitochondrial proteome. Biochim Biophys Acta-Bioenerg 1659(2–3):212–220 (Special issue)Google Scholar
  59. Gabaldon T, Snel B, van Zimmeren F, Memrika W, Tabak H, Huynen MA (2006) Origin and evolution of the peroxisomal proteome. Biol Direct 1:8 (23 March 2006)Google Scholar
  60. Germot A, Philippe H, LeGuyader H (1996) Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc Natl Acad Sci USA 93:14614–14617PubMedCrossRefGoogle Scholar
  61. Gibor A, Izawa M (1963) The DNA content of the chloroplasts of Acetabularia. Proc Natl Acad Sci USA 50(6):1164–1169PubMedCrossRefGoogle Scholar
  62. Gibor A, Granick S (1964) Plastids and mitochondria: inheritable systems. Science 145:890–897PubMedCrossRefGoogle Scholar
  63. Giles RE, Blanc H, Cann HM Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77(11):6715–6719PubMedCrossRefGoogle Scholar
  64. Goosen NK, Horemans AMC, Hillebrand SJW, Stumm CK, Vogels GD (1988) Cultivation of the sapropelic ciliate Plagiopyla nasuta Stein and isolation of the endosymbiont Methanobacterium formicicum. Arch Microbiol 150:165–170CrossRefGoogle Scholar
  65. Goosen NK, van der Drift C, Stumm CK, Vogels GD (1990a) End products of metabolism in the anaerobic ciliate Trimyema compressum. FEMS Microbiol Lett 69:171–175CrossRefGoogle Scholar
  66. Goosen NK, Wagener S, Stumm CK (1990b) A comparison of 2 strains of the anaerobic ciliate Trimyema compressum. Arch Microbiol 153:187–192CrossRefGoogle Scholar
  67. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283(5407):1476–1481PubMedCrossRefGoogle Scholar
  68. Gray MW, Lang BF, Burger G (2004) Mitochondria of protists. Annu Rev Genet 38:477–524PubMedCrossRefGoogle Scholar
  69. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  70. Hackstein JHP (1997) Eukaryotic molecular biodiversity: systematic approaches for the assessment of symbiotic associations. Anton Leeuw 72:63–76CrossRefGoogle Scholar
  71. Hackstein JHP (2005) Eukaryotic Fe-hydrogenases—old eukaryotic heritage or adaptive acquisitions? Biochem Soc Trans 33:47–50PubMedCrossRefGoogle Scholar
  72. Hackstein JHP, Akhmanova A, Boxma B, Harhangi HR, Voncken FG (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol 7:441–447PubMedCrossRefGoogle Scholar
  73. Hackstein JHP, Akhmanova A, Voncken F, van Hoek A, van Alen T, Boxma B, Moon-van der Staay SY, van der Staay G, Leunissen J, Huynen M, Rosenberg J, Veenhuis M (2001) Hydrogenosomes: convergent adaptations of mitochondria to anaerobic environments. Zoology 104:290–302PubMedCrossRefGoogle Scholar
  74. Hackstein JHP, van Alen TA, Rosenberg J (2006) Methane production by terrestrial arthropods. In: König H, Varma A (eds) Intestinal microorganisms of termites and other invertebrates. Soil biology, vol 6, manual for soil analysis. Springer, Berlin Heidelberg New York, pp 155–180Google Scholar
  75. Haferkamp I, Hackstein JHP, Voncken FGJ, Schmit G, Tjaden J (2002) Functional integration of mitochondrial and hydrogenosomal ADP/ATP carriers in the Escherichia coli membrane reveals different biochemical characteristics for plants, mammals and anaerobic chytrids. Eur J Biochem 269(13):3172–3181PubMedCrossRefGoogle Scholar
  76. Haig D, Henikoff S (2004) Genomes and evolution. Deciphering the genomic palimpsest. Curr Opin Genet Dev 14:599–602CrossRefGoogle Scholar
  77. Henze K, Martin W (2003) Evolutionary biology: essence of mitochondria. Nature 426(6963):127–128PubMedCrossRefGoogle Scholar
  78. Hildebrand F (1908) Über Sämlinge von C. Adami. Ber D Deutsch Bot Ges 26A:590Google Scholar
  79. Horner DS, Hirt RP, Embley TM (1999) A single eubacterial origin of eukaryotic pyruvate: ferredoxin oxidoreductase genes: implications for the evolution of anaerobic eukaryotes. Mol Biol Evol 16(9):1280–1291PubMedGoogle Scholar
  80. Horner DS, Foster PG, Embley TM (2000) Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol Biol Evol 17:1695–1705PubMedGoogle Scholar
  81. Horner DS, Embley TM (2001) Chaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes. Mol Biol Evol 18:1970–1975PubMedGoogle Scholar
  82. Horner DS, Heil B, Happe T, Embley TM (2002) Iron hydrogenases—ancient enzymes in modern eukaryotes. Trends Biochem Sci 27:148–153PubMedCrossRefGoogle Scholar
  83. Hrdy I, Hirt RP, Dolezal P, Bardonova L, Foster PG, Tachezy J, Embley TM (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618–622PubMedCrossRefGoogle Scholar
  84. Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76PubMedCrossRefGoogle Scholar
  85. Huang CY, Ayliffe MA, Timmis JN (2004) Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco. Proc Natl Acad Sci USA 101(26):9710–9715PubMedCrossRefGoogle Scholar
  86. Huang CY, Grunheit N, Ahmadinejad N, Timmis JN, Martin W (2005) Mutational decay and age of chloroplast and mitochondrial genomes. Plant Physiol 138:1723–1733PubMedCrossRefGoogle Scholar
  87. Jacob F (1977) Evolution and tinkering. Science 196(4295):1161–1166PubMedCrossRefGoogle Scholar
  88. Jacob F (2001) Complexity and tinkering. Ann NY Acad Sci 929:71–73PubMedCrossRefGoogle Scholar
  89. Karlberg O, Canback B, Kurland CG, Andersson SG (2000) The dual origin of the yeast mitochondrial proteome. Yeast 17(3):170–187PubMedCrossRefGoogle Scholar
  90. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivares CP (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–453PubMedCrossRefGoogle Scholar
  91. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW (2005) The tree of eukaryotes. Trends Ecol Evol 20(12):670–676PubMedCrossRefGoogle Scholar
  92. Kerscher S, Drose S, Zwicker K, Zickermann V, Brandt U (2002) Yarrowia lipolytica, a yeast genetic system to study mitochondrial complex I. Biochim Biophys Acta 1555(1–3):83–91PubMedGoogle Scholar
  93. Knoll AH, Carroll SB (1999) Early animal evolution: emerging views from comparative biology and geology. Science 284(5423):2129–2137PubMedCrossRefGoogle Scholar
  94. Kurland CG, Andersson SGE (2000) Origin and evolution of the mitochondrial proteome. Mol Biol Rev 64:786–820CrossRefGoogle Scholar
  95. Lang BF, Burger G, OKelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387(6632):493–497PubMedCrossRefGoogle Scholar
  96. Lang BF, Brinkmann H, Koski L, Fujishima M, Goertz HD, Burger G (2005) On the origin of mitochondria and Rickettsia-related eukaryotic endosymbionts. Jpn J Protozool 38(2):171–183Google Scholar
  97. Leon-Avila G, Tovar J (2004) Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiology 150:1245–1250PubMedCrossRefGoogle Scholar
  98. Leroch M (2006) Molekulare, biochemische und physiologische Eigenschaften von Transportproteinen aus der MCF (mitochondrial carrier family) in Pflanzen und Protisten. PhD Thesis, Technische Universität Kaiserslautern, GermanyGoogle Scholar
  99. Leroch M, Kirchberger S, Haferkamp I, Wahl M, Neuhaus HE, Tjaden J (2005) Identification and characterization of a novel plastidic adenine nucleotide uniporter from Solanum tuberosum. J Biol Chem 280:17992–18000PubMedCrossRefGoogle Scholar
  100. Lill R, Mühlenhoff U (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30:133–141PubMedCrossRefGoogle Scholar
  101. Lindmark DG, Müller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 248:7724–7728PubMedGoogle Scholar
  102. Lopez-Garcia P, Moreira D (1999) Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci 24(3):88–93PubMedCrossRefGoogle Scholar
  103. Lopez-Garcia P, Moreira D (2006) Selective forces for the origin of the eukaryotic nucleus. Bioessays 28(5):525–533PubMedCrossRefGoogle Scholar
  104. Mai ZM, Ghosh S, Frisardi M, Rosenthal B, Rogers R, Samuelson J (1999) Hsp60 is targeted to a cryptic mitochondrion-derived organelle (“crypton”) in the microaerophilic protozoan parasite Entamoeba histolytica. Mol Cell Biol 19(3):2198–2205PubMedGoogle Scholar
  105. Margulis L (1993) Symbiosis in cell evolution. 2nd edn. WH Freeman and Company, New YorkGoogle Scholar
  106. Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41PubMedCrossRefGoogle Scholar
  107. Martin W, Koonin EV (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440:41–45PubMedCrossRefGoogle Scholar
  108. Martin W (2005) The missing link between hydrogenosomes and mitochondria. Trends Mirobiol 13:457–459CrossRefGoogle Scholar
  109. Martin W, Hoffmeister M, Rotte C, Henze K (2001) An overview of endosymbiotic models for the origins of eukaryotes, their ATP producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol Chem 382:1521–1539PubMedCrossRefGoogle Scholar
  110. Mendel G (1865) Versuche über Pflanzenhybriden. Verhandl. Naturf. Verein Brünn 4:3–47 (1986) (English translation by W. Bateson in Peters, JA Classic papers in genetics. Prentice-Hall Inc., Englewood Cliffs, NJ, USA, 1959; pp 1–20)Google Scholar
  111. Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralblatt 25(18):593–604 (Annotated English translation by William Martin and Klaus V. Kowallik in Eur J Phycol 34(3):287–295, 1999)Google Scholar
  112. Moreira D, Lopez-Garcia P (1998) Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J Mol Evol 47(5):517–530PubMedCrossRefGoogle Scholar
  113. Müller M (1993) The hydrogenosome. J Gen Microbiol 139:2879–2889PubMedGoogle Scholar
  114. Müller M (1998) Enzymes and compartmentalization of core energy metabolism of anaerobic protists—a special case in eukaryotic evolution? In: Coombs GH, Vickerman K, Sleigh MA, Warren A (eds) Evolutionary relationships among protozoa. The Systematics Association, special volume series 56. Kluwer Academic Publishers, Dordrecht, Boston London, pp 109–132Google Scholar
  115. Nass MMK, Nass S (1963a) Intramitochondrial fibers with DNA characteristics. I. Fixation and electron staining reactions. J Cell Biol 19:593–611CrossRefGoogle Scholar
  116. Nass S, Nass MMK (1963b) Intramitochondrial fibres with DNA characteristics. II. Enzymatic and other treatments. J Cell Biol 19:613–629CrossRefGoogle Scholar
  117. Nass MMK, Nass S, Afzelius BA (1965) The general occurrence of mitochondrial DNA. Exp Cell Res 37:516–539PubMedCrossRefGoogle Scholar
  118. Palmieri F (1994) Mitochondrial carrier proteins. FEBS Lett 346:48–54PubMedCrossRefGoogle Scholar
  119. Palmer JD (2003) The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol 39(1):4–11CrossRefGoogle Scholar
  120. Portier P (1918) Les symbiotes. Masson, ParisGoogle Scholar
  121. Regoes A, Zourmpanou D, Leon-Avila G, van der Giezen M, Tovar J, Hehl AB (2005) Protein import, replication, and inheritance of a vestigial mitochondrion. J Biol Chem 280:30557–30563PubMedCrossRefGoogle Scholar
  122. Reichert AS, Neupert W (2004) Mitochondriomics or what makes us breathe. Trends Genet 20:555–562PubMedCrossRefGoogle Scholar
  123. Renner O (1922) Eiplasma und Pollenschlauchplasma als Vererbungsträger bei den Oenotheren. Z Induct Abstamm-U Vererbungs l 27:235–237Google Scholar
  124. Renner O (1924) Die Scheckung der Oenotherenbastarde. Biol Zentralb 44:309Google Scholar
  125. Renner O (1934) Die pflanzlichen Plastiden als selbständige Elemente der genetischen Konstitution. Ber Sächs Akad Wiss Math-Phys Kl 86:241–266Google Scholar
  126. Renner O (1936a) Zur Entwicklungsgeschichte randpanaschierter Formern von Sambucus, Veronica, Pelargonium, Spirea, Chlorophytum. Flora 130:154Google Scholar
  127. Renner O (1936b) Zur Kenntnis der nichtmendelnden Buntheit der Laublätter. Flora 130:218Google Scholar
  128. Ribero S, Golding GB (1998) The mosaic nature of the eukaryotic nucleus. Mol Biol Evol 15:779–788Google Scholar
  129. Rivera MC, Lake JA (2004) The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431:152–155PubMedCrossRefGoogle Scholar
  130. Rivera MC, Jain R, Moore JE, Lake JA (1998) Genomic evidence for two functionally distinct gene classes. PNAS 95:6239–6244PubMedCrossRefGoogle Scholar
  131. Rivière L, van Weelden SWH, Glass P, Vegh P, Coustou V, Biran M, van Hellemond JJ, Bringaud F, Tielens AGM, Boshart M (2004) Acetyl: succinate CoA-transferase in procyclic Trypanosoma brucei—gene identification and role in carbohydrate metabolism. J Biol Chem 279:45337–45346PubMedCrossRefGoogle Scholar
  132. Rodriguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, Bohnert HJ, Philippe H, Lang BF (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15(4):1325–1330PubMedCrossRefGoogle Scholar
  133. Roger AJ (1999) Reconstructing early events in eukaryotic evolution. Am Nat 154:S146–S163PubMedCrossRefGoogle Scholar
  134. Rotte C, Henze K, Müller M, Martin W (2000) Origins of hydrogenosomes and mitochondria—commentary. Curr Opin Microbiol 3:481–486PubMedCrossRefGoogle Scholar
  135. Sagan L (1967) The origin of mitosing cells. J Theoret Biol 14:225–274CrossRefGoogle Scholar
  136. Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science 283:1488–1493PubMedCrossRefGoogle Scholar
  137. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B, Rehling P, Pfanner N, Meisinger C (2003) The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci USA 100:13207–13212PubMedCrossRefGoogle Scholar
  138. Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147:195–197PubMedCrossRefGoogle Scholar
  139. Smeitink JA, Zeviani M, Turnbull DM, Jacobs HT (2006) Mitochondrial medicine: a metabolic perspective on the pathology of oxidative phosphorylation disorders. Cell Metab 3(1):9–13PubMedCrossRefGoogle Scholar
  140. Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci USA 100(15):8828–8833PubMedCrossRefGoogle Scholar
  141. Stubbe W (1959) Genetische Analyse des Zusammenwirkens von Genom und Plastom bei Oenothera. Z Vererbungsl 90:288–298CrossRefGoogle Scholar
  142. Tielens AG, Rotte C, van Hellemond JJ, Martin W (2002) Mitochondria as we don’t know them. Trends Biochem Sci 27:564–572PubMedCrossRefGoogle Scholar
  143. Tjaden J, Haferkamp I, Boxma B, Tielens AGM, Huynen M, Hackstein JHP (2004) A divergent ADP/ATP carrier in the hydrogenosomes of Trichomonas gallinae argues for an independent origin of these organelles. Mol Microbiol 51:1439–1446PubMedCrossRefGoogle Scholar
  144. Tilney-Basset RAE (1963) Genetics and plastid physiology in Pelargonium. Heredity 18:265CrossRefGoogle Scholar
  145. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135PubMedCrossRefGoogle Scholar
  146. Tovar J, Fischer A, Clark CG (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol 32:1013–1021PubMedCrossRefGoogle Scholar
  147. Tovar J, Leon-Avila G, Sanchez LB, Sutak R, Tachezy J, van der Giezen M, Hernandez Müller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron sulfur protein maturation. Nature 426:172–176PubMedCrossRefGoogle Scholar
  148. Vanacova S, Liston DR, Tachezy J, Johnson PJ (2003) Molecular biology of the amitochondriate parasites, Giardia intestinalis, Entamoeba histolytica and Trichomonas vaginalis. Int J Parasitol 33:235–255PubMedCrossRefGoogle Scholar
  149. van Bruggen JJA, Stumm CK, Vogels GD (1983) Symbiosis of methanogenic bacteria and sapropelic protozoa. Arch Microbiol 136:89–95CrossRefGoogle Scholar
  150. van Bruggen JJA, Zwart KB, van Assema RM, Stumm CK, Vogels GD (1984) Methanobacterium formicicum, an endosymbiont of the anaerobic ciliate Metopus striatus McMurrich. Arch Microbiol 139:1–7CrossRefGoogle Scholar
  151. van Bruggen JJA, Zwart KB, Herman JGF, van Hove EM, Assema RM, Stumm CK, Vogels GD (1986) Isolation and characterization of Methanoplanus endosymbiosus sp.nov., an endosymbiont of the marine sapropelic ciliate Metopus contortus Quennerstedt. Arch Microbiol 144:367–374CrossRefGoogle Scholar
  152. van der Giezen M, Sjollema KA, Artz RRE, Alkema W, Prins RA (1997) Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS Lett 408:147–150PubMedCrossRefGoogle Scholar
  153. van der Giezen M, Slotboom DJ, Horner DS, Dyal PL, Harding M, Xue GP, Embley TM, Kunji ERS (2002) Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. Embo J 21:572–579PubMedCrossRefGoogle Scholar
  154. van der Giezen M, Birdsey GM, Horner DS, Lucocq J, Dyal PL, Benchimol M, Danpure CJ, Embley TM (2003) Fungal hydrogenosomes contain mitochondrial heat-shock proteins. Mol Biol Evol 20:1051–1061PubMedCrossRefGoogle Scholar
  155. van der Giezen M, Cox S, Tovar J (2004) The iron-sulfur cluster assembly genes iscS and iscU of Entamoeba histolytica were acquired by horizontal gene transfer. BMC Evol Biol 4; Art. No. 7 February 20 2004Google Scholar
  156. van der Giezen M, Tovar J, Clark CG (2005) Mitochondrion-derived organelles in protists and fungi. Int Rev Cytol 244:175–225PubMedCrossRefGoogle Scholar
  157. van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6:525–530PubMedCrossRefGoogle Scholar
  158. van der Giezen M, Leon-Avila G, Tovar J (2005) Characterization of chaperonin 10 (Cpn10) from the intestinal human pathogen Entamoeba histolytica. Microbiol-SGM 151:3107–3115CrossRefGoogle Scholar
  159. van Hellemond JJ, Opperdoes FR, Tielens AGM (1998) Trypanosomatidae produce acetate via a mitochondrial acetate: succinate CoA transferase. Proc Natl Acad Sci USA 95:3036–3041PubMedCrossRefGoogle Scholar
  160. van Hoek AHAM, van Alen TA, Sprakel VSI, Hackstein JHP, Vogels GD (1998) Evolution of anaerobic ciliates from the gastrointestinal tract: phylogenetic analysis of the ribosomal repeat from Nyctotherus ovalis and its relatives. Mol Biol Evol 15:1195–1206PubMedGoogle Scholar
  161. van Hoek AHAM, Sprakel VSI, van Alen TA, Theuvenet APR, Vogels GD, Hackstein JHP (1999) Voltage dependent reversal of anodic galvanotaxis in Nyctotherus ovalis. J Euk Microbiol 46:427–433PubMedCrossRefGoogle Scholar
  162. van Hoek AHAM, Akhmanova AS, Huynen M, Hackstein JHP (2000a) A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol Biol Evol 17:202–206Google Scholar
  163. van Hoek AHAM, van Alen TA, Sprakel VSI, Leunissen JAM, Brigge T, Vogels GD, Hackstein JHP (2000b) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 17:251–258Google Scholar
  164. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501PubMedGoogle Scholar
  165. Vivares CP, Gouy M, Thomaratb F, Météniera G (2002) Functional and evolutionary analysis of a eukaryotic parasitic genome. Curr Opin Microbiol 5:499–505PubMedCrossRefGoogle Scholar
  166. Voncken FGJ (2001) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Thesis Nijmegen. ISBN 90-9014868-x. Ponsen and Looien BV, Wageningen, The NetherlandsGoogle Scholar
  167. Voncken FGJ, Boxma B, Tjaden J, Akhmanova AS, Huynen M, Verbeek F, Tielens AGM, Haferkamp I, Neuhaus HE, Vogels G, Veenhuis M, Hackstein JHP (2002a) Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp. Mol Microbiol 44:1441–1454CrossRefGoogle Scholar
  168. Voncken FGJ, Boxma B, van Hoek AHAM, Akhmanova AS, Vogels GD, Huynen M, Veenhuis M, Hackstein JHP (2002b) A hydrogenosomal [Fe]-hydrogenase from the anaerobic chytrid Neocallimastix sp L2. Gene 284:103–112CrossRefGoogle Scholar
  169. von Dohlen CD, Kohler S, Alsop ST, McManus WR (2001) Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 412(6845):433–436CrossRefGoogle Scholar
  170. Wallace DC (1989) Mitochondrial DNA mutations and neuromuscular disease. Trends Genet 5(1):1–13Google Scholar
  171. Wallin IE (1925) On the nature of mitochondria. IX. Demonstration of the bacterial nature of mitochondria. Am J Anat 36:131–146CrossRefGoogle Scholar
  172. Wallin IE (1927) Symbionticism and the origin of species. Williams and Wilkins, BaltimoreGoogle Scholar
  173. Williams BAP, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–869PubMedCrossRefGoogle Scholar
  174. Winkler HH, Neuhaus HE (1999) Non-mitochondrial ATP transport. Trends Biochem Sci 24:64–68PubMedCrossRefGoogle Scholar
  175. Yaffe MP (1999) The machinery of mitochondrial inheritance and behavior. Science 283:1493–1497PubMedCrossRefGoogle Scholar
  176. Yarlett N, Hann AC, Lloyd D, Williams A (1981) Hydrogenosomes in the rumen protozoan Dasytricha ruminantium Schuberg. Biochem J 200(2):365–372PubMedGoogle Scholar
  177. Yarlett N, Coleman GS, Williams AG, Lloyd D (1984) Hydrogenosomes in known species of rumen entodiniomorphid protozoa. FEMS Microbiol Lett 21(1):15–19CrossRefGoogle Scholar
  178. Yarlett N (2004) Anaerobic protists and hidden mitochondria. Microbiol-SGM 150:127–129CrossRefGoogle Scholar
  179. Yarlett N, Hackstein JHP (2005) Hydrogenosomes: one organelle, multiple origins. Bioscience 55:657–668CrossRefGoogle Scholar
  180. Zillig W, Klenk HP, Palm P, Leffers H, Pühler G, Gropp F, Garret RA (1989) Did eukaryotes originate by a fusion event? Endocyt Cell Res 6:1–25Google Scholar
  181. Zwart KB, Goosen NK, van Schijndel MW, Broers CAM, Stumm CK, Vogels GD (1988) Cytochemical-localization of hydrogenase activity in the anaerobic protozoa Trichomonas vaginalis, Plagiopyla nasuta and Trimyema compressum. J Gen Microbiol 134:2165–2170Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Johannes H. P. Hackstein
    • 1
    Email author
  • Joachim Tjaden
    • 2
  • Martijn Huynen
    • 3
  1. 1.Department of Evolutionary Microbiology, Faculty of ScienceRadboud University NijmegenED NijmegenThe Netherlands
  2. 2.Department of Plant PhysiologyUniversity of KaiserslauternKaiserslauternGermany
  3. 3.Nijmegen Centre for Molecular Life Sciences (NCMLS) and Centre for Molecular and Biomolecular InformaticsED NijmegenThe Netherlands

Personalised recommendations