Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1470, 2006, Pages 1055-1067

  Embley, T Martin ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Anaerobic eukaryote evolution; Hydrogenosomes; Mitochondria; Mitosomes

Indexed keywords

ENDOSYMBIONT; EUKARYOTE; EVOLUTION; HOST-SYMBIONT INTERACTION; MITOCHONDRION;

EUKARYOTA;

HYDROGENASE; IRON HYDROGENASE; IRON SULFUR PROTEIN; PYRUVATE SYNTHASE;

ANAEROBIC GROWTH; ENZYMOLOGY; EUKARYOTIC CELL; EVOLUTION; GENETICS; METABOLISM; MITOCHONDRION; PHYLOGENY; PHYSIOLOGY; REVIEW;

ANAEROBIOSIS; EUKARYOTIC CELLS; EVOLUTION; HYDROGENASE; IRON-SULFUR PROTEINS; MITOCHONDRIA; PHYLOGENY; PYRUVATE SYNTHASE;

EID: 33747810433     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1844     Document Type: Review

References (144)

1. Abrahamsen, M. S. et al. 2004 Complete genome sequence of the apicomplexan Cryptosporidium parvum. Science 304, 441-445. (doi:10.1126/science. 1094786)
2. Adams, K. L. & Palmer, J. D. 2003 Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol. Phylogenet. Evol. 29, 380-395. (doi:10.1016/S1055-7903(03)00194-5)
3. Adl, S. M. et al. 2005 The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399-451. (doi:10.1111/j.1550-7408.2005.00053.x)
4. Akhmanova, A., Voncken, F., vanAlen, T., vanHoek, A., Boxma, B., Vogels, G., Veenhuiss, M. & Hackstein, J. H. P. 1998 A hydrogenosome with a genome. Nature 396, 527-528. (doi:10.1038/25023)
5. Ali, V., Shigeta, Y., Tokumoto, U., Takahashi, Y. & Nozaki, T. 2004 An intestinal parasitic protist Entamoeba histolytica, possesses a non-redundant nitrogen fixation-like system for iron-sulfur cluster assembly under anaerobic conditions. J. Biol. Chem. 279, 16 863-16 874. (doi:10.1074/ jbc.M313314200)
6. Arisue, N., Hasegawa, M. & Hashimoto, T. 2005 Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. Mol. Biol. Evol. 22, 409-420. (doi:10.1093/molbev/ msi023)
7. Bakatselou, C., Kidgell, C. & Graham Clark, C. 2000 A mitochondrial-type hsp70 gene of Entamoeba histolytica. Mol. Biochem. Parasitol. 110, 177-182. (doi:10.1016/ S0166-6851(00)00264-4)
8. Balk, J., Pierik, A. J., Netz, D. J., Muhlenhoff, U. & Lill, R. 2004 The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J. 23, 2105-2115. (doi:10.1038/sj.emboj. 7600216)
9. Balk, J., Pierik, A. J., Aguilar Netza, D. J., Muhlenhoff, U. & Lill, R. 2005 Nar1p, a conserved eukaryotic protein with similarity to Fe-only hydrogenases, functions in cytosolic iron-sulphur protein biogenesis. Biochem. Soc. Trans. 33, 86-89. (doi:10.1042/BST0330086)
10. Bapteste, E. et al. 2002 The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc. Natl Acad. Sci. USA 99, 1414-1419. (doi:10.1073/pnas.032662799)
11. Barton, R. M. & Worman, H. J. 1999 Prenylated prelamin A interacts with Narf, a novel nuclear protein. J. Biol. Chem. 274, 30 008-30 018. (doi:10.1074/jbc.274.42.30008)
12. Bernard, C. & Fenchel, T. 1994 Chemosensory behavior of Strombidium purpureum, an anaerobic oligotrich with endosymbiotic purple nonsulfur bacteria. J. Eukaryot. Microbiol. 41, 391-396.
13. Boorstein, W. R., Ziegelhoffer, T. & Craig, E. A. 1994 Molecular evolution of the HSP70 multigene family. J. Mol. Evol. 38, 1-7. (doi:10.1007/BF00175490)
14. Boxma, B. et al. 2005 An anaerobic mitochondrion that produces hydrogen. Nature 434, 74-79. (doi:10.1038/ nature03343)
15. Bozner, P. 1997 Immunological detection and subcellular localization of HSP70 and HSP60 homologues in Trichomonas vaginalis. J. Parasitol. 83, 224-229.
16. Brown, D. M., Upcroft, J. A., Edwards, M. R. & Upcroft, P. 1998 Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis. Int. J. Parasitol. 28, 149-164. (doi:10.1016/S0020-7519(97)00172-0)
17. Bui, E. T. N. & Johnson, P. J. 1996 Identification and characterisation of [Fe]-hydrogenases in the hydrogenosome of Trichomonas vaginalis. Mol. Biochem. Parasitol. 76, 305-310. (doi:10.1016/0166-6851(96) 02567-4)
18. Bui, E. T. N., Bradley, P. J. & Johnson, P. J. 1996 A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl Acad. Sci. USA 93, 9651-9656. (doi:10.1073/pnas.93.18.9651)
19. Cavalier-Smith, T. 1983a A 6 kingdom classification and a unified phylogeny. In Endocytobiology II (ed. W. Schwemmler & H. E. A. Schenk), pp. 1027-1034. Berlin, Germany: De Gruyter.
20. Cavalier-Smith, T. 1983b Endosymbiotic origin of the mitochondrial envelope. In Endocytobiology II (ed. W. Schwemmler & H. E. A. Schenk), pp. 265-279. Berlin, Germany: De Gruyter.
21. Cavalier-Smith, T. 1987a Eukaryotes with no mitochondria. Nature 326, 332-333. (doi:10.1038/326332a0)
22. Cavalier-Smith, T. 1987b The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. In Endocytobiology III (ed. J. L. Lee & J. F. Frederick), pp. 55-71. New York, NY: New York Academy of Sciences.
23. Cavalier-Smith, T. 2002 The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int. J. Syst. Evol. Microbiol. 52, 297-354.
24. Cavalier-Smith, T. 2006 Cell evolution and Earth history: stasis and revolution. Phil. Trans. R. Soc. B 361, 969-1006. (doi:10.1098/rstb.2006.1842)
25. Chan, K. W. et al. 2005 A Novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr. Biol. 15, 737-742. (doi:10.1016/ j.cub.2005.02.068)
26. Clark, C. G. & Roger, A. J. 1995 Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl Acad. Sci. USA 92, 6518-6521.
27. Clemens, D. L. & Johnson, P. J. 2000 Failure to detect DNA in hydrogenosomes of Trichomonas vaginalis by nick translation and immunomicroscopy. Mol. Biochem. Parasitol. 106, 307-313. (doi:10.1016/S0166- 6851(99) 00220-0)
28. Darwin, C. 1859 The origin of species. Penguin Classics, 1985 reprint of 1859 edition. London: Penguin Books.
29. Davidson, E. A., van der Giezen, M., Homer, D. S., Embley, T. M. & Howe, C. J. 2002 An [Fe]-hydrogenase from the anaerobic hydrogenosome-containing fungus Neocallimas-tix frontalis L2. GENE 296, 45-52. (doi:10.1016/S0378- 1119(02)00873-9)
30. Dolezal, P., Smid, O., Rada, P., Zubacova, Z., Bursac, D., Sutak, R., Nebesarova, J., Lithgow, T. & Tachezy, J. 2005 Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc. Natl Acad. Sci. USA 102, 10924-10929. (doi:10.1073/pnas. 0500349102)
31. Doolittle, W. F. 1998 You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14, 307-311. (doi:10. 1016/50168-9525(98)01494-2)
32. Dyall, S. B. & Johnson, P. J. 2000 Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr. Opin. Microbiol. 3, 404-411. (doi:10.1016/S1369-5274(00)00112-0)
33. Dyall, S. D., Koehler, C. M., Delgadillo-Correa, M. G., Bradley, P. J., Plumper, E., Leuenberger, D., Turck, C. W. & Johnson, P. J. 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. (doi:10.1128/MCB.20.7.2488-2497.2000)
34. Dyall, S. D., Brown, M. T. & Johnson, P. J. 2004a Ancient invasions: from endosymbionts to organelles. Science 304, 253-257. (doi:10.1126/science. 1094884)
35. Dyall, S. D., Yan, W., Delgadillo-Correa, M. G., Lunceford, A., Loo, J. A., Clarke, C. F. & Johnson, P. J. 2004b Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431, 1103-1107. (doi:10. 1038/nature02990)
36. Embley, T. M. & Martin, W. 2006 Eukaryotic evolution, changes and challenges. Nature 440, 623-630. (doi:10. 1038/nature04546)
37. Embley, T. M., Finlay, B. J., Dyal, P. L., Hirt, R. P., Wilkinson, M. & Williams, A. G. 1995 Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc. R. Soc. B 262, 87-93.
38. Embley, T. M., Homer, D. S. & Hirt, R. P. 1997 Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria? Trends Ecol. Evol. 12, 437-441. (doi:10.1016/S0169-5347(97)01208-1)
39. Embley, T. M., van der Giezen, M., Horner, D. S., Dyal, P. L., Bell, S. & Foster, P. G. 2003a Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55, 387-395.
40. Embley, T. M., van der Giezen, M., Horner, D. S., Dyal, P. L. & Foster, P. 2003b Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. Phil. Trans. R. Soc. B 358, 191-203. (doi:10.1098/rstb. 2002.1190)
41. Emelyanov, V. V. 2003 Phylogenetic affinity of a Giardia lamblia cysteine desulfurase conforms to canonical pattern of mitochondrial ancestry. FEMS Microbiol. Lett. 226, 257-266. (doi:10.1016/S0378-1097(03)00598-6)
42. Esser, C. et al. 2004 A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 1643-1660. (doi:10.1093/molbev/msh160)
43. Esteban, G., Guhl, B. E., Ken, J. C., Embley, T. M. & Finlay, B. J. 1993 Cyclidium porcatum n.sp.: a free-living anaerobic scuticociliate containing a stable complex of hydrogenosomes, eubacteria and archaeobacteria. Eur. J. Protistol. 29, 262-270.
44. Fast, N. M. & Keeling, P. J. 2001 Alpha and beta subunits of pyruvate dehydrogenase E1 from the microsporidian Nosema locustae: mitochondrion-derived carbon metabolism in microsporidia. Mol. Biochem. Parasitol. 117, 201-209. (doi:10.1016/S0166-6851(01)00356-5)
45. Fenchel, T. 1993 There are more small than large species? Oikos 68, 375-378.
46. Fenchel, T. & Bernard, C. 1993a Endosymbiotic purple non-sulphur bacteria in an anaerobic ciliated protozoon. FEMS Microbiol. Ecol. 110, 21-25.
47. Fenchel, T. & Bernard, C. 1993b A purple protist. Nature 362, 300. (doi:10.1038/362300a0)
48. Fenchel, T. & Finlay, B. J. 1995 Ecology and evolution in anoxic worlds. Oxford series in ecology and evolution. Oxford, UK: Oxford University Press.
49. Germot, A., Philippe, H. & Le Guyader, H. 1996 Presence of a mitochondrial-type HSP70 in Trichomonas suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc. Natl Acad. Sci. USA 93, 14614-14617. (doi:10. 1073/pnas.93.25.14614)
50. Germot, A., Philippe, H. & Le Guyader, H. 1997 Loss of mitochondria in microsporidia: evidence from a mitochondrial-type HSP-70 in Nosema locustae. Mol. Biochem. Parasitol. 87, 159-168. (doi:10.1016/S0166-6851(97) 00064-9)
51. Goksoyr, J. 1967 Evolution of eucaryotic cells. Nature 214, 1161.
52. Gray, M. W. 2005 Evolutionary biology: the hydrogenosome's murky past. Nature 434, 29-31. (doi:10.1038/ 434029a)
53. Gray, M. W., Burger, G. & Lang, B. F. 2001 The origin and early evolution of mitochondria. Genome Biol. 2, 10 181-10 185. (doi:10.1186/gb-2001- 2-6-reviews1018)
54. Gray, M. W., Lang, B. F. & Burger, G. 2004 Mitochondria of protists. Annu. Rev. Genet. 38, 477-524. (doi:10.1146/ annurev.genet.37.110801.142526)
55. Hashimoto, T., Nakamura, Y., Kamaishi, T. & Hasegawa, M. 1997 Early evolution of eukaryotes inferred from the amino acid sequences of elongation factors 1a and 2. Arch. Protistenkd. 148, 287-295.
56. Hirt, R. P., Healy, B., Vossbrinck, C. R., Canning, E. U. & Embley, T. M. 1997 A mitochondrial HSP70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr. Biol. 7, 995-998. (doi:10.1016/S0960-9822(06)00420-9)
57. Hirt, R. P., Logsdon, J. M., Healy, B., Dorey, M. W., Doolittle, W. F. & Embley, T. M. 1999 Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl Acad. Sci. USA 96, 580-585. (doi:10.1073/pnas.96.2.580)
58. Ho, S. Y. W. & Jermiin, L. S. 2004 Tracing the decay of the historical signal in biological sequence data. Syst. Biol. 53, 623-637. (doi:10.1080/10635150490503035)
59. Horner, D. S. & Embley, T. M. 2001 Chaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes. Mol. Biol. Evol. 18, 1970-1975.
60. Horner, D., Hirt, R. P., Kilvington, S., Lloyd, D. & Embley, T. M. 1996 Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc. R. Soc. B 263, 1053-1059.
61. Horner, D. S., Hirt, R. P. & Embley, T. M. 1999 A single eubacterial origin of eukaryotic pyruvate:ferredoxin oxidoreductase genes: implications for the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 16, 1280-1291.
62. Horner, D. S., Foster, P. G. & Embley, T. M. 2000 Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 17, 1695-1709.
63. Horner, D. S., Heil, B., Happe, T. & Embley, T. M. 2002 Iron hydrogenases-ancient enzymes in modern eukaryotes. Trends Biochem. Sci. 27, 148-153. (doi:10.1016/S0968-0004(01)02053-9)
64. Hrdy, I. & Müller, M. 1995a Primary structure and eubacterial relationships of the pyruvate:ferredoxin oxidoreductase of the amitochondriate eukaryote Trichomonas vaginalis. J. Mol. Evol. 41, 388-396.
65. Hrdy, I. & Müller, M. 1995b Primary structure of the hydrogenosomal malic enzyme of Trichomonas vaginalis and its relationship to homologous enzymes. J. Eukaryot. Microbiol. 42, 593-603.
66. Hrdy, I., Hirt, R. P., Dolezal, P., Bardonova, L., Foster, P. G., Tachezy, J. & Embley, T. M. 2004 Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432, 618-622. (doi:10. 1038/nature03149)
67. Inagaki, Y., Susko, E., Fast, N. M. & Roger, A. J. 2004 Covarion shifts cause a long-branch attraction artifact that unites microsporidia and archaebacteria in EF-1alpha phylogenies. Mol. Biol. Evol. 21, 1340-1349. (doi:10. 1093/molbev/msh130)
68. John, P. & Whatley, F. R. 1975 Paracoccus denitricans and the evolutionary origin of the mitochondrion. Nature 254, 495-498. (doi:10.1038/254495a0)
69. Katinka, M. D. et al. 2001 Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450-453. (doi:10.1038/35106579)
70. Keeling, P. J., Luker, M. A. & Palmer, J. D. 2000 Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17, 23-31.
71. Klingenberg, M. 1985 The ADP/ATP carrier in mitochondrial membranes. In The enzymes of biological membranes (ed. A. N. Martonosi), pp. 511-553. New York, NY: Plenum Press.
72. Knight, J. 2004 Giardia: not so special, after all? Nature 429, 236-237. (doi:10.1038/429236a)
73. Kunji, E. R. 2004 The role and structure of mitochondrial carriers. FEBS Lett. 564, 239-244. (doi:10.1016/S0014-5793(04)00242-X)
74. Kurland, C. G. & Andersson, S. G. 2000 Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64, 786-820. (doi:10.1128/MMBR.64.4.786-820.2000)
75. LaGier, M. J., Tachezy, J., Stejskal, F., Kutisova, K. & Keithly, J. S. 2003 Mitochondrial-type iron-sulfur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum. Microbiology 149, 3519-3530. (doi:10.1099/mic.0.26365-0)
76. Leipe, D. D., Gunderson, J. H., Nerad, T. A. & Sogin, M. L. 1993 Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol. Biochem. Parasitol. 59, 41-48. (doi:10.1016/0166-6851(93)90005-1)
77. Lill, R. & Muhlenhoff, U. 2005 Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem. Sci. 30, 133-141. (doi:10. 1016/j.tibs.2005.01.006)
78. Lill, R., Diekert, K., Kaut, A., Lange, H., Pelzer, W., Prohl, C. & Kispal, G. 1999 The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins. Biol. Chem. 380, 1157-1166. (doi:10.1515/BC.1999.147)
79. Lindmark, D. G. & Müller, M. 1973 Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate, Tritrichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem. 248, 7724-7728.
80. Lloyd, D., Ralphs, J. R. & Harris, J. C. 2002 Giardia intestinalis, a eukaryote without hydrogenosomes, produces hydrogen. Microbiology 148, 727-733.
81. Loftus, B. et al. 2005 The genome of the protist parasite Entamoeba histolytica. Nature 433, 865-868. (doi:10.1038/ nature03291)
82. Margulis, L., Dolan, M. F. & Whiteside, J. H. 2005 "Imperfections and oddities" in the origin of the nucleus. Paleobiology 31, 175-191. (doi:10.1666/0094-8373(2005) 031[0175:IAOITO]2.0.CO;2)
83. Martin, W. 2005 The missing link between hydrogenosomes and mitochondria. Trends Microbiol. 13, 457-459. (doi:10. 1016/j.tim.2005.08.005)
84. Martin, W. & Müller, M. 1998 The hydrogen hypothesis for the first eukaryote. Nature 392, 37-41. (doi:10.1038/ 32096)
85. Moreira, D. & LopezGarcia, P. 1998 Symbiosis between methanogenic archaea and deha-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J. Mol. Evol. 47, 517-530. (doi:10.1007/PL00006408)
86. Morrison, H. G., Roger, A. J., Nystul, T. G., Gillin, F. D. & Sogin, M. L. 2001 Giardia lamblia expresses a proteo-bacterial-like DnaK homolog. Mol. Biol. Evol. 18, 530-541.
87. Müller, M. 1993 The hydrogenosome. J. Gen. Microbiol. 139, 2879-2889.
88. Müller, M. 2003 Energy metabolism. Part 1: Anaerobic protozoa. In Molecular medical parasitolgy (ed. J. J. Marr, T. W. Nilsen & R. W. Komuniecki), pp. 125-139. Amsterdam, The Netherlands: Academic Press.
89. Nixon, J. E., Field, J., McArthur, A. G., Sogin, M. L., Yarlett, N., Loftus, B. J. & Samuelson, J. 2003 Iron-dependent hydrogenases of Entamoeba histolytica and Giardia lamblia: activity of the recombinant entamoebic enzyme and evidence for lateral gene transfer. Biol. Bull. 204, 1-9.
90. Owen, R. 1843 Lectures on the comparative physiology of the invertebrate animals. London: Longman, Brown, Green and Longmans.
91. Patterson, D. J. & Sogin, M. L. 1992 Eukaryotic origins and protistan diversity. In The origin and evolution of the cell (ed. H. Hartman & K. Matsuno), pp. 13-46. Singapore: World Scientific.
92. Penny, D., McComish, B. J., Charleston, M. A. & Hendy, M. D. 2001 Mathematical elegance with biochemical realism: the covarion model of molecular evolution. J. Mol. Evol. 53, 711-723. (doi:10.1007/s002390010258)
93. Peyretaillade, E., Broussole, V., Peyret, P., Metenier, G., Gouy, M. & Vivares, C. P. 1998 Microsporidia, amitochondriate protists, possess a 70-kDa heat shock protein gene of mitochondrial origin. Mol. Biol. Evol. 15, 683-689.
94. Pfanner, N. & Geissler, A. 2001 Versatility of the mitochondrial protein import machinery. Nat. Rev. Mol. Cell Biol. 2, 339-349. (doi:10.1038/35073006)
95. Philippe, H. & Adoutte, A. 1998 The molecular phylogeny of protozoa: solid facts and uncertainties. In Evolutionary relationships among protozoa (ed. G. H. Coombs, K. Vickerman, M. A. Sleigh & A. Warren), pp. 25-56. Dordrecht, The Netherlands: Kluwer Academic Publishers.
96. Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Muller, M. & Le Guyader, H. 2000 Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc. R. Soc. B 267, 1213-1221. (doi:10.1098/rspb.2000.1130)
97. Plumper, E., Bradley, P. J. & Johnson, P. J. 1998 Implications of protein import on the origin of hydrogenosomes. Protist 149, 303-311.
98. Reeves, R. E. 1984 Metabolism of Entamoeba histolytica Schaudinn, 1903. Adv. Parasitol. 23, 105-142.
99. Reeves, R. E., Warren, L. G., Suskind, B. & Lo, H. S. 1977 An energy conserving pyruvate to acetate pathway in Entamoeba histolytica. J. Biol. Chem. 252, 726-731.
100. Regoes, A., Zourmpanou, D., Leon-Avila, G., van der Giezen, M., Tovar, J. & Hehl, A. B. 2005 Protein import, replication and inheritance of a vestigial mitochondrion. J. Biol. Chem. 280, 30557-30563. (doi:10.1074/jbc. M500787200)
101. Reichert, A. S. & Neupert, W. 2004 Mitochondriomics or what makes us breathe. Trends Genet. 20, 555-562. (doi:10.1016/j.tig.2004.08.012)
102. Ribeiro, S. & Golding, G. B. 1998 The mosaic nature of the eukaryotic nucleus. Mol. Biol. Evol. 15, 779-788.
103. Riordan, C. E., Ault, J. G., Langreth, S. G. & Keithly, J. S. 2003 Cryptosporidium parvum Cpn60 targets a relict organelle. Curr. Genet. 44, 138-147. (doi:10.1007/ S00294-003-0432-1)
104. Rivera, M. C. & Lake, J. A. 2004 The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152-155. (doi:10.1038/nature02848)
105. Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. 1998 Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 6239-6244. (doi:10.1073/pnas.95.11.6239)
106. Rodriguez, M. A., Garcia-Perez, R. M., Mendoza, L., Sanchez, T., Guillen, N. & Orozco, E. 1998 The pyruvate:ferredoxin oxidoreductase enzyme is located in the plasma membrane and in a cytoplasmic structure in Entamoeba. Microb. Pathog. 25, 1-10. (doi:10.1006/mpat. 1998.0202)
107. Roger, A. J. & Hug, L. A. 2006 The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation. Phil. Trans. R. Soc. B 361, 1039-1054. (doi:10.1098/rstb.2006.1845)
108. Roger, A. J., Clark, C. G. & Doolittle, W. F. 1996 A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc. Natl Acad. Sci. USA 93, 14 618-14 622. (doi:10.1073/pnas.93.25. 14618)
109. Roger, A. J., Svard, S. G., Tovar, J., Clark, C. G., Smith, M. W., Gillin, F. D. & Sogin, M. L. 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. (doi:10.1073/pnas.95.1.229)
110. Rotte, C., Stejskal, F., Zhu, G., Keithly, J. S. & Martin, W. 2001 Pyruvate:NADP oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol. Biol. Evol. 18, 710-720.
111. Searcy, D. G. 1992 Origin of mitochondria and chloroplasts from sulfur-based symbioses. In The origin and evolution of the cell (ed. H. H. Matsuno & K. Matsuno), pp. 47-78. Singapore: World Scientific Press.
112. Siddall, M. E., Hong, H. & Desser, S. S. 1992 Phylogenetic analysis of the Diplomonadida (Wenyon, 1926) Brugerolle, 1975: evidence for heterochrony in protozoa and against Giardia lamblia as a "missing link". J. Protozool. 39, 361-367.
113. Slapeta, J. & Keithly, J. S. 2004 Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria. Eukaryot. Cell 3, 483-494. (doi:10. 1128/EC.3.2.483-494.2004)
114. Sogin, M. L. 1997 History assignment: when was the mitochondrion founded? Curr. Opin. Genet. Dev. 7, 792-799. (doi:10.1016/S0959-437X(97)80042-1)
115. Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. & Peattie, D. A. 1989 Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243, 75-77.
116. Stiller, J. W. & Hall, B. D. 1999 Long-branch attraction and the rDNA model of early eukaryotic evolution. Mol. Biol. Evol. 16, 1270-1279.
117. Sutak, R., Dolezal, P., Fiumera, H. L., Hrdy, I., Dancis, A., Delgadillo-Correa, M., Johnson, P. J., Muller, M. & Tachezy, J. 2004 Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc. Natl Acad. Sci. USA 101, 10368-10373. (doi:10.1073/pnas.0401319101)
118. Tachezy, J., Sanchez, L. B. & Muller, M. 2001 Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol. Biol. Evol. 18, 1919-1928.
119. Thomarat, F., Vivares, C. P. & Gouy, M. 2004 Phylogenetic analysis of the complete genome sequence of Encephalitozoon cuniculi supports the fungal origin of microsporidia and reveals a high frequency of fast-evolving genes. J. Mol. Evol. 59, 780-791. (doi:10.1007/ S00239-004-2673-0)
120. Timmis, J. N., Ayliffe, M. A., Huang, C. Y. & Martin, W. 2004 Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123-135. (doi:10.1038/nrg1271)
121. Tjaden, J., Haferkamp, I., Boxma, B., Tielens, A. G., Huynen, M. & Hackstein, J. H. 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. (doi:10.1111/ j.1365-2958.2004.03918.x)
122. Tovar, J., Fischer, A. & Clark, C. G. 1999 The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32, 1013-1021. (doi:10.1046/j.1365-2958.1999.01414. x)
123. Tovar, J., Leon-Avila, G., Sanchez, L. B., Sutak, R., Tachezy, J., van der Giezen, M., Hernandez, M., Muller, M. & Lucocq, J. M. 2003 Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426, 172-176. (doi:10.1038/nature01945)
124. Townson, S. M., Upcroft, J. A. & Upcroft, P. 1996 Characterisation and purification of pyruvate:ferredoxin oxidoreductase from Giardia duodenalis. Mol. Biochem. Parasitol. 79, 183-193. (doi:10.1016/0166-6851(96) 02661-8)
125. van der Giezen, M., Sjollema, K. A., Artz, R. R. E., Alkema, W. & Prins, R. A. 1997 Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS Lett. 408, 147-150. (doi:10.1016/S0014-5793(97)00409-2)
126. van der Giezen, M., Slotboom, D. J., Horner, D. S., Dyal, P. L., Harding, M., Xue, G. P., Embley, T. M. & Kunji, E. R. 2002 Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. EMBO J. 21, 572-579. (doi:10.1093/ emboj/21.4.572)
127. van der Giezen, M., Birdsey, G. M., Horner, D. S., Lucocq, J., Dyal, P. L., Benchimol, M., Danpure, C. J. & Embley, T. M. 2003 Fungal hydrogenosomes contain mitochondrial heat-shock proteins. Mol. Biol. Evol. 20, 1051-1061. (doi:10.1093/molbev/msg103)
128. 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. (doi:10.1186/1471-2148-4-7)
129. van der Giezen, M., Tovar, J. & Clark, C. G. 2005 Mitochondrion-derived organelles in protists and fungi. Int. Rev. Cytol. 244, 175-225.
130. Vellai, T. & Vida, G. 1999 The origin of eukaryotes: the difference between prokaryotic and eukaryotic cells. Proc. R. Soc. B 266, 1571-1577. (doi:10.1098/rspb.1999.0817)
131. Vellai, T., Takacs, K. & Vida, G. 1998 A new aspect to the origin and evolution of eukaryotes. J. Mol. Evol. 46, 499-507. (doi:10.1007/PL00006331)
132. Viale, A. M. & Arakaki, A. K. 1994 The chaperone connection to the origins of the eukaryotic organelles. FEBS Lett. 341, 146-151. (doi:10.1016/0014-5793(94)80446-X)
133. Vivares, C. P., Gouy, M., Thomarat, F. & Metenier, G. 2002 Functional and evolutionary analysis of a eukaryotic parasitic genome. Curr. Opin. Microbiol. 5, 499-505.
134. Voncken, F. et al. 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. (doi:10.1046/j.1365-2958. 2002.02959.x)
135. Voncken, F. G., Boxma, B., van Hoek, A. H., Akhmanova, A. S., Vogels, G. D., Huynen, M., Veenhuis, M. & Hackstein, J. H. 2002b A hydrogenosomal [Fe]-hydrogenase from the anaerobic chytrid Neocallimastix sp. L2. Gene 284, 103-112. (doi:10.1016/S0378-1119(02) 00388-8)
136. Vossbrinck, C. R., Maddox, J. V., Friedman, S., Debrunner-Vossbrinck, B. A. & Woese, C. R. 1987 Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326, 411-414. (doi:10.1038/ 326411a0)
137. Whatley, J. M., John, P. & Whatley, F. R. 1979 From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc. R. Soc. B. 204, 165-187.
138. Williams, B. A., Hirt, R. P., Lucocq, J. M. & Embley, T. M. 2002 A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865-869. (doi:10. 1038/nature00949)
139. Woese, C. R. 1977 Endosymbionts and mitochondrial origins. J. Mol. Evol. 10, 93-96. (doi:10.1007/ BFO1751802)
140. Wolters, J. 1991 The troublesome parasites-molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. Biosystems 25, 75-83. (doi:10. 1016/0303-2647(91)90014-C)
141. Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J. & Woese, C. R. 1985 Mitochondrial origins. Proc. Natl Acad. Sci. USA 82, 4443-4447.
142. Yarlett, N., Lloyd, D. & Williams, A. 1981 Hydrogenosomes in the rumen protozoon Dasytricha ruminantium Schuberg. Biochem. J. 200, 365-372.
143. Yarlett, N., Coleman, G. S., Williams, A. G. & Lloyd, D. 1984 Hydrogenosomes in known species of rumen entodiniomorphid protozoa. FEMS Microbiol. Lett. 21, 15-19.
144. Yarlett, N., Orpin, C. G., Munn, E. A., Yarlett, N. C. & Greenwood, C. A. 1986 Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem. J. 236, 729-739.