Hydrogenosomes (and related organelles, either) are not the same

Origin of Mitochondria and Hydrogenosomes

Volumn , Issue , 2007, Pages 135-159

  Hackstein, Johannes H P ^a   Tjaden, Joachim ^b   Koopman, Werner ^c   Huynen, Martijn ^d  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b University of Koblenz Landau   (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78649971950     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-540-38502-8_7     Document Type: Chapter

References (125)

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 304:441-445.
2. 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 396:527-528.
3. 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 30:1017-1027.
4. Akhmanova A, Voncken FGJ, Hosea KM, Harhangi H, Keltjens JT, op den Camp HJ, Vogels GD, Hackstein JHP (1999) A hydrogenosome with pyruvate formate-lyase: Anaerobic chytrid fungi use an alternative route for pyruvate catabolism. Mol Microbiol 32:1103-1114.
5. Amiri H, Karlberg O, Andersson SG (2003) Deep origin of plastid/parasite ATP/ADP translocases. J Mol Evol 56:137-150.
6. Andersson SGE, Kurland CG (1999) Origin of mitochondria and hydrogenosomes. Curr Opin Microbiol 2:535-541.
7. Balk J, Lill R (2004) The cell's cookbook for iron-sulfur clusters: recipes for fool's gold? Chem Bio Chem 5:1044-1049.
8. Benchimol M, Engelke F (2003) Hydrogenosome behavior during the cell cycle in Tritrichomonas foetus. Biol Cell 95:283-293.
9. Benchimol M, Johnson PJ, de Souza W (1996) Morphogenesis of the hydrogenosome: An ultrastructural study. Biol Cell 87:197-205.
10. Berry S (2003) Endosymbiosis and the design of eukaryotic electron transport. Biochim Biophys Acta 1606:57-72.
11. Biagini GA, Finlay BJ, Lloyd D (1997a) Evolution of the hydrogenosome. FEMS Microbiol Lett 155:133-140.
12. Biagini GA, Hayes AJ, Suller MTE, Winters C, Finlay BJ, Lloyd D (1997b) Hydrogenosomes of Metopus contortus physiologically resemble mitochondria. Microbiology 143:1623-1629.
13. 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 279:46686-46691.
14. Bowman BH, Taylor JW, Brownlee AG, Lee J, Lu SD, White TJ (1992) Molecular evolution of the fungi: relationship of the Basidiomycetes, Ascomycetes, and Chytridiomycetes. Mol Biol Evol 9:285-296.
15. 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 51:1389-1399.
16. 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 434:74-79.
17. Bui ETN, Bradley PJ, Johnson PJ (1996) A common evolutionary origin for the mitochondria and hydrogenosomes. Proc Natl Acad Sci USA 93:9651-9656.
18. Bullerwell CE, Lang BF (2005) Fungal evolution: The case of the vanishing mitochondrion. Curr Opin Microbiol 8:362-369.
19. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: Anything goes. Trends Genet 19:709-716.
20. 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 15:737-742.
21. Clark CG, Roger AJ (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci USA 92:6518-6521.
22. Clemens DL, Johnson PJ (2000) Failure to detect DNA in hydrogenosomes of Trichomonas vaginalis by nick translation and immunomicroscopy. Mol Biochem Parasitol 106:307-313.
23. Coombs GH, Hackstein JHP (1995) Anaerobic protists and anaerobic ecosystems. In: Brugerolle G, Mignot J-P (eds) Protistological actualities. Proceedings of the second European congress of protistology, Clermont-Ferrand, France. Universite Blaise Pascal, Clermont- Ferrand, pp 90-101.
24. Cotter D, Guda P, Fahy E, Subramaniam S (2004) MitoProteome: mitochondrial protein sequence database and annotation system. Nucleic Acids Res 32:D463-D467.
25. del Arco A, Satrustegui J (2005) New mitochondrial carriers: An overview. Cell Mol Life Sci 62:2204-2227.
26. Dyall SD, Johnson PJ (2000) Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr Opin Microbiol 3:404-411.
27. 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 20:2488-2497.
28. 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 278:30548-30561.
29. Dyall SD, Brown, MT, Johnson PJ (2004a) Ancient invasions: from endosymbionts to organelles. Science 304:253-257.
30. 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 431:1103-1107.
31. Embley TM, Martin W (1998) A hydrogen-producing mitochondrion. Nature 396:517-519.
32. 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 Biol Sci 262:87-93.
33. Embley TM, Horner DA, Hirt RP (1997) Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria? Trends Ecol Evol 12:437-441.
34. Embley TM, van der Giezen M, Horner DS, Dyal PL, Bell S, Foster PG (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55:387-395.
35. 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 alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol Biol Evol 21:1643-1660.
36. Feagin JE (2000) Mitochondrial genome diversity in parasites. Int J Parasit 30:371-390.
37. Fenchel T, Finlay BJ (1995) Ecology and evolution in anoxic worlds. Oxford University Press, Oxford.
38. Gabaldon T (2005) Origin and evolution of the mitochondrial proteome. Applications for protein function prediction in the eukaryotes. Thesis, Nijmegen.
39. Gabaldon T, Huynen MA (2003) Reconstruction of the proto-mitochondrial metabolism. Science 301:609-609.
40. Gabaldon T, Huynen MA (2004) Shaping the mitochondrial proteome. Biochim Biophys Acta 1659:212-220.
41. 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.
42. Gelius-Dietrich G, Henze K (2004) Pyruvate formate lyase (PFL) and PFL activating enzyme in the chytrid fungus Neocallimastix frontalis: A free-radical enzyme system conserved across divergent eukaryotic lineages. J Eukaryot Microbiol 51:456-463.
43. 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 93:14614-1467.
44. Germot A, Philippe H, LeGuyader H (1997) Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol Biochem Parasitol 87:159-168.
45. Gijzen HJ, Broers CAM, Barughare M, Stumm CK (1991) Methanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalis in the cockroach hindgut. Appl Environ Microbiol 57:1630-1634.
46. Goosen NK, Horemans AMC, Hillebrand SJW, Stumm CK, Vogels GD (1988) Arch Microbiol 150:165-170.
47. Goosen NK, van der Drift C, Stumm CK, Vogels GD (1990a) End products of metabolism in the anaerobic ciliate Trimyema compressum. FEMS Microbiol Lett 69:171-175.
48. Goosen NK, Wagener S, Stumm CK (1990b) A comparison of 2 strains of the anaerobic ciliate Trimyema compressum Arch Microbiol 153:187-192.
49. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science: 283:1476-1481.
50. Hackstein JHP (2005) Eukaryotic Fe-hydrogenases - old eukaryotic heritage or adaptive acquisitions? Biochem Soc Trans 33:47-50.
51. Hackstein JHP, Akhmanova A, Boxma B, Harhangi HR, Voncken FG (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol 7:441-447.
52. 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 104:290-302.
53. Hackstein JHP, van Hoek AHAM, Leunissen JAM, Huynen M (2002) Anaerobic ciliates and their methanogenic endosymbionts. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer, Dordrecht, pp 451-464.
54. 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 269:3172-3181.
55. Horner DS, Foster PG, Embley TM (2000) Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol Biol Evol 17:1695-1705.
56. Horner DS, Embley TM (2001) Chaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes. Mol Biol Evol 18:1970-1975.
57. Horner DS, Heil B, Happe T, Embley TM (2002) Iron hydrogenases - Ancient enzymes in modern eukaryotes. Trends Biochem Sci 27:148-153.
58. 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 432:618-622.
59. Humphreys M, Ralphs J, Durrant L, Lloyd D (1998) Confocal laser scanning microscopy of trichomonads: Hydrogenosomes store calcium and show a membrane potential. Eur J Protistol 34:356-362.
60. 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 414:450-453.
61. 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: 387:493-497.
62. Leon-Avila G, Tovar J (2004) Mitosomes of Entamoeba histolytica are abundant mitochondrion- related remnant organelles that lack a detectable organellar genome. Microbiology 150:1245-1250.
63. 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, Germany.
64. 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 280:17992-18000.
65. Lill R, Mühlenhoff U (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30:133-141.
66. Lindmark DG, Muller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 248:7724-7728.
67. Martin W (2005) The missing link between hydrogenosomes and mitochondria. Trends Mirobiol 13:457-459.
68. Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37-41.
69. 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 382:1521-1539.
70. Marvin-Sikkema FD, Lahpor GA, Kraak MN, Gottschal JC, Prins RA (1992) Characterization of an anaerobic fungus from llama faeces. J Gen Microbiol 138:2235-2241.
71. Marvin-Sikkema FD, Kraak MN, Veenhuis M, Gottschal JC, Prins RA (1993) The hydrogenosomal enzyme hydrogenase from the anaerobic fungus Neocallimastix sp. L2 is recognized by antibodies directed against the C-terminal microbody targeting signal SKL. Eur J Cell Biol 61:86-91.
72. Marvin-Sikkema FD, Driessen AJM, Gottschal JC, Prins RA (1994) Metabolic energy generation in hydrogenosomes of the anaerobic fungus Neocallimastix: Evidence for a functional relatioship with mitochondria. Mycol Res 98:205-212.
73. Müller M (1993) The hydrogenosome. J Gen Microbiol 139:2879-2889.
74. 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, Dordrecht, pp 109-132.
75. Nasirudeen AMA, Tan KSW (2004) Isolation and characterization of the mitochondrion-like organelle from Blastocystis hominis. J Microbiol Methods 58:101-109.
76. Nosek J, Tomaska L (2003) Mitochondrial genome diversity: evolution of the molecular architecture and replication strategy. Curr Genet 44:73-84.
77. Orpin CG (1994) Anaerobic fungi: Taxonomy, biology and distribution in nature. In: Mountfort DO, Orpin CG (eds) Anaerobic fungi. Dekker, New York, pp 1-45.
78. Palmieri F (1994) Mitochondrial carrier proteins. FEBS Lett 346:48-54.
79. Paquin B, Forget L, Roewer I, Lang BF (1995) Molecular phylogeny of Allomyces macrogynus: congruency between nuclear ribosomal RNA- And mitochondrial protein-based trees. J Mol Evol 41:657-665.
80. Paquin B, Lang BF (1996) The mitochondrial DNA of Allomyces macrogynus: The complete genomic sequence from an ancestral fungus. J Mol Biol 255:688-701.
81. Ragan MA, Chapman DJ (1978) A biochemical phylogeny of the protists. Academic, New York.
82. 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 280:30557-30563.
83. Riordan CE, Ault JG, Langreth SG, Keithley JG (2003) Cryptosporidium parvum Cpn60 targets a relict organelle. Curr Genet 44:138-147.
84. 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 279:45337-45346.
85. Roger AJ (1999) Reconstructing early events in eukaryotic evolution. Am Nat 154:S146-S163.
86. Roger AJ, Svard SG, Tovar J, Clark CG, Smith MW, Gillin FD, Sogin ML (1998) 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 USA 95:229-234.
87. Rotte C, Henze K, Müller M, Martin W (2000) Origins of hydrogenosomes and mitochondria - commentary. Curr Opin Microbiol 3:481-486.
88. Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science 283:1488-1493.
89. 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 100:13207-13212.
90. Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147:195-197.
91. Teunissen MJ, Smits AA, Op den Camp HJ, Huis in't Veld JH, Vogels GD (1991) Fermentation of cellulose and production of cellulolytic and xylanolytic enzymes by anaerobic fungi from ruminant and non-ruminant herbivores. Arch Microbiol 156:290-296.
92. Tielens AG, Rotte C, van Hellemond JJ, Martin W (2002) Mitochondria as we don't know them. Trends Biochem Sci 27:564-572.
93. 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 51:1439-1446.
94. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: Organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123-135.
95. Tovar J, Fischer A, Clark CG (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol 32:1013-1021.
96. 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 fuction in iron sulfur protein maturation. Nature 426:172-176.
97. Turner AC, Lushbaugh WB (1991) Three aspecific ATPases in Trichomonas vaginalis. Comp Biochem Physiol B 100:691-696.
98. 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 33:235-255.
99. van Bruggen JJA, Stumm CK, Vogels GD (1983) Symbiosis of methanogenic bacteria and sapropelic protozoa. Arch Microbiol 136:89-95.
100. 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 139:1-7.
101. 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 144:367-374.
102. 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 408:147-150.
103. 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 21:572-579.
104. 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 20:1051-1061.
105. 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 4:7.
106. van der Giezen M, Tovar J, Clark CG (2005) Mitochondrion-derived organelles in protists and fungi. Int Rev Cytol 244:175-225.
107. van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6:525-530.
108. van Hellemond JJ, Opperdoes FR, Tielens AGM (1998) Trypanosomatidae produce acetate via a mitochondrial acetate:succinate CoA transferase. Proc Natl Acad Sci USA 95:3036-3041.
109. 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 15:1195-1206.
110. 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 46:427-433.
111. van Hoek AHAM, Akhmanova AS, Huynen M, Hackstein JHP (2000a) A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol Biol Evol 17:202-206.
112. 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 17:251-258.
113. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455-501.
114. Vivares CP, Gouy M, Thomaratb F, Météniera G (2002) Functional and evolutionary analysis of a eukaryotic parasitic genome. Curr Opin Microbiol 5:499-505.
115. Vogels GD, Hoppe WF, Stumm CK (1980) Association of methanogenic bacteria with rumen ciliates. Appl Environ Microbiol 40:608-612.
116. Voncken FGJ (2001) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Thesis, Nijmegen. Ponsen and Looien, Wageningen.
117. 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 44:1441-1454.
118. 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 284:103-112.
119. Williams BAP, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865-869.
120. Winkler HH, Neuhaus HE (1999) Non-mitochondrial ATP transport. Trends Biochem Sci 24:64-68.
121. Yaffe MP (1999) The machinery of mitochondrial inheritance and behavior. Science 283:1493-1497.
122. Yarlett N (1994) Fermentation product generation in rumen chytridiomycetes. In: Mountfort DO, Orpin CG (eds) Anaerobic fungi. Dekker, New York, pp 129-146.
123. Yarlett N (2004) Anaerobic protists and hidden mitochondria. Microbiology 150:127-129.
124. Yarlett N, Hackstein JHP (2005) Hydrogenosomes: one organelle, multiple origins. Bioscience 55:657-668.
125. 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 134:2165-2170.