Iron-sulfur proteins and iron-sulfur cluster assembly in organisms with hydrogenosomes and mitosomes

Origin of Mitochondria and Hydrogenosomes

Volumn , Issue , 2007, Pages 105-133

  Tachezy, Jan ^a   Doležal, Pavel ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 36549035976     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-540-38502-8_6     Document Type: Chapter

References (139)

1. Adam AC, Bornhovd C, Prokisch H, Neupert W, Hell K (2005) The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J 25:174-183.
2. Adam RD (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14:447-475.
3. Akhmanova A, Voncken F, van Alen T, van Hoek A, Boxma B, Vogels G, Veenhuiss M, Hackstein JHP (1998) A hydrogenosome with a genome. Nature 396:527-528.
4. 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 ironsulfur cluster assembly under anaerobic conditions. J Biol Chem 279:16863-16874.
5. Alves R, Herrero E, Sorribas A (2004) Predictive reconstruction of the mitochondrial ironsulfur cluster assembly metabolism. II. Role of glutaredoxin Grx5. Proteins Struct Funct Bioinform 57:481-492.
6. 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 13:94-104.
7. Arisue N, Sachez LB, Weiss LM, Muller M, Hashimoto T (2002) Mitochondrial-type hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitol Int 51:9-16.
8. Balk J, Pierik AJ, Guilar Netz DJ, 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.
9. Best AA, Morrison HG, McArthur AG, Sogin ML, Olsen GJ (2004) Evolution of eukaryotic transcription: insights from the genome of Giardia lamblia. Genome Res 14:1537-1547.
10. Besteiro S, Barrett MP, Riviere L, Bringaud F (2005) Energy generation in insect stages of Trypanosoma brucei: metabolism in flux. Trends Parasitol 21:185-191.
11. Boxma B, de Graaf RM, van der Staay GWM, van Alen TA, Ricard G, Gabaldon T, van Hoek AHAM, Moon-van der Staay S, 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.
12. Broers CAM (1992) Anaerobic psalteriomonad amoeboflagellates. Thesis, University of Nijmegen, Nijmegen.
13. Brul S, Veltman RH, Lombardo MC, Vogels GD (1994) Molecular cloning of hydrogenosomal ferredoxin cDNA from the anaerobic amoeboflagellate Psalteriomonas lanterna. Biochim Biophys Acta 1183:544-546.
14. Bui ET, Bradley PJ, Johnson PJ (1996) A common evolutionary origin for mitochondria and hydrogenosomes. Proc Natl Acad Sci USA 93:9651-9656.
15. Campuzano V, Montermini L, Molto MD, Pianese L, Cossee M, Cavalcanti F, Monros E, Rodius F, Duclos F, Monticelli A, Zara F, Canizares J, Koutnikova H, Bidichandani SI, Gellera C, Brice A, Trouillas P, DeMichele G, Filla A, DeFrutos R, Palau F, Patel PI, DiDonato S, Mandel JL, Cocozza S, Koenig M, Pandolfo M (1996) Friedreich's ataxia: Autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271:1423-1427.
16. Cavalier-Smith T (1987a) Eukaryotes with no mitochondria [news]. Nature 326:332-333.
17. Cavalier-Smith T (1987b) The origin of eukaryotic and archaebacterial cells. Ann N Y Acad Sci 503:17-54.
18. Čerkasovova A, Lukasǒva G, Čerkasov J, Kulda J (1973) Biochemical characterization of large granule fraction of Tritrichomonas foetus (KV1 strain). J Protozool 20:537.
19. 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.
20. Crossnoe CR, Germanas JP, LeMagueres P, Mustata G, Krause KL (2002) The crystal structure of Trichomonas vaginalis ferredoxin provides insight into metronidazole activation. J Mol Biol 318:503-518.
21. Dacks JB, Davis, LAM, Sjogren AM, Andersoon JO, Roger AJ, Doolittle WF (2003) Evidence for cryptic Golgi in putatively 'Golgi-lacking' lineages. Proc Biol Sci 270:S168-171.
22. Dailey HA, Dailey TA, Wu CK, Medlock AE, Wang KF, Rose JP, Wang BC (2000) Ferrochelatase at the millennium: structures, mechanisms and [2Fe-2S] clusters. Cell Mol Life Sci 57:1909-1926.
23. Davidson EA, van der Giezen M, Horner DS, Embley TM, Howe CJ (2002) An [Fe] hydrogenase from the anaerobic hydrogenosome-containing fungus Neocallimastix frontalis L2. Gene 296:45-52.
24. Decottignies A, Goffeau A (1997) Complete inventory of the yeast ABC proteins. Nat Genet 15:137-145.
25. Doležal P, Smid O, Rada P, Zubcǒva Z, Bursac D, Šut'ak R, Nebesarǒva 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.
26. Dong J-S, Lai R, Nielsen K, Fekete CA, Qiu H-F, Hinnebusch AG (2004) The essential ATPbinding cassette protein Rli1 functions in translation by promoting preinitiation complex assembly. J Biol Chem 274:42157-42168.
27. Dutkiewicz R, Schilke B, Knieszner H, Walter W, Craig EA, Marszalek J (2003) Ssq1, a mitochondrial Hsp70 involved in iron-sulfur (Fe/S) center biogenesis - similarities to and differences from its bacterial counterpart. J Biol Chem 278:29719-29727.
28. Dyall SD, Johnson PJ (2000) Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr Opin Microbiol 3:404-411.
29. Dyall SD, Brown MT, Johnson PJ (2004a) Ancient invasions: from endosymbionts to organelles. Science 304:253-257.
30. Dyall SD, Yan W, Gadillo-Correa MG, Lunceford A, Loo JA, Clarke CF, Johnson PJ (2004b) Nonmitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431:1103-1107.
31. 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.
32. Embley TM, van der Giezen M, Horner DS, Dyal PL, Bell S, Foster PG (2003a) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55:387-395.
33. Embley TM, van der Giezen M, Horner DS, Dyal PL, Foster P (2003b) Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. Philos Trans R Soc Lond B Biol Sci 358:191-202.
34. Emelyanov VV (2003) Phylogenetic affinity of a Giardia lamblia cysteine desulfurase conforms to canonical pattern of mitochondrial ancestry. FEMS Microbiol Lett 226:257-266.
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. Fenchel T, Finlay BJ (1994) The evolution of life without oxygen. Am Sci 82:22-29.
37. Finel M (1998) Organization and evolution of structural elements within complex I. Biochim Biophys Acta 1364:112-121.
38. Jan Tachezy and Pavel Doležal Gakh O, Adamec J, Gacy AM, Twesten RD, Owen WG, Isaya G (2002) Physical evidence that yeast frataxin is an iron storage protein. Biochemistry 41:6798-6804.
39. 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 93:14614-14617.
40. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476-1481.
41. Grieshaber MK, Volkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33-53.
42. Hackstein JHP, Akhmanova A, Boxma B, Harhangi HR, Voncken FGJ (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol 7:441-447.
43. Han KL, Yong TS, Ryu JS, Hwang UW, Park SJ (2004) Identification of the hybrid cluster protein, HCP, from amitochondriate eukaryotes and its phylogenetic implications. J Microbiol Biotechnol 14:134-139.
44. Hashimoto T (1998) Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc Natl Acad Sci USA 95:6860-6865.
45. Hausmann A, Guilar Netz DJ, Balk J, Pierik AJ, Muhlenhoff U, Lill R (2005) The eukaryotic P loop NTPase Nbp35: An essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc Natl Acad Sci USA 102:3266-3271.
46. Horner DS, Foster PG, Embley TM (2000) Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol Biol Evol 17:1695-1709.
47. Horner DS, Heil B, Happe T, Embley TM (2002) Iron hydrogenases - Ancient enzymes in modern eukaryotes. Trends Biochem Sci 27:148-153.
48. Horner DS, Hirt RP, Kilvington S, Lloyd D, Embley TM (1996) Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc R Soc Lond B Biol Sci 263:1053-1059.
49. Hrdý I, Hirt RP, Doležal P, Bardonǒva L, Foster PG, Tachezy J, Embley TM (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618-622.
50. Huber C, Wachtershauser G (1997) Activated acetic acid by carbon fixation on (Fe, Ni)S under primordial conditions. Science 276:245-247.
51. Jacobson MR, Cash VL, Weiss MC, Laird NF, Newton WE, Dean DR (1989) Biochemical and genetic analysis of the nif USVWZM cluster from Azotobacter vinelandii. Mol Gen Genet 219:49-57.
52. Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74:247-281.
53. Johnson PJ, d'Oliveira CE, Gorrell TE, Muller M (1990) Molecular analysis of the hydrogenosomal ferredoxin of the anaerobic protist Trichomonas vaginalis. Proc Natl Acad Sci USA 87:6097-6101.
54. Kapazoglou A, Mould RM, Gray JC (2000) Assembly of the Rieske iron-sulphur protein into the cytochrome bf complex in thylakoid membranes of isolated pea chloroplasts. Eur J Biochem 267:352-360.
55. 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.
56. Keithly JS, Langreth SG, Buttle KF, Mannella CA (2005) Electron tomographic and ultrastructural analysis of the Cryptosporidium parvum relict mitochondrion, its associated membranes, and organelles. J Eukaryot Microbiol 52:132-140.
57. Kennedy C, Dean D (1992) The nifU, nifS and nifV gene products are required for activity of all three nitrogenases of Azotobacter vinelandii. Mol Gen Genet 231:494-498.
58. Kispal G, Csere P, Prohl C, Lill R (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18:3981-3989.
59. Kispal G, Sipos K, Lange H, Fekete Z, Bedekovics T, Janaky T, Bassler J, Guilar Netz DJ, Balk J, Rotte C, Lill R (2005) Biogenesis of cytosolic ribosomes requires the essential iron-sulphur protein Rli1p and mitochondria. EMBO J 24:589-598.
60. Kita K, Hirawake H, Takamiya S (1997) Cytochromes in the respiratory chain of helminth mitochondria. Int J Parasitol 27:617-630.
61. Kulda J (1999) Trichomonads, hydrogenosomes and drug resistance. Int J Parasitol 29:199-212.
62. Kurland CG, Andersson SGE (2000) Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev 64:786-820.
63. LaGier MJ, Tachezy J, Stejskal F, Kutisǒva K, Keithly JS (2003) Mitochondrial-type iron-sulfur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum. Microbiol-SGM 149:3519-3530.
64. Land KM, Gadillo-Correa MG, Tachezy J, Vaňacǒva S, Hsieh CL, Šut'ak R and Johnson PJ (2004) Targeted gene replacement of a ferredoxin gene in Trichomonas vaginalis does not lead to metronidazole resistance. Mol Microbiol 51:115-122.
65. Lange H, Lisowsky T, Gerber J, Muhlenhoff U, Kispal G, Lill R (2001) An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep 2:715-720.
66. 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.
67. Lill R, Kispal G (2000) Maturation of cellular Fe-S proteins: An essential function of mitochondria. Trends Biochem Sci 25:352-356.
68. Lill R, Muhlenhoff U (2005) Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem Sci 30:133-141.
69. 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.
70. 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.
71. Lindmark DG, Muller M, Shio H (1975) Hydrogenosomes in Trichomonas vaginalis. J Parasitol 61:552-554.
72. Lloyd D, Harris JC (2002) Giardia: highly evolved parasite or early branching eukaryote? Trends Microbiol 10:122-127.
73. Lloyd D, Ralphs JR Harris JC (2002) Giardia intestinalis, a eukaryote without hydrogenosomes, produces hydrogen. Microbiology 148:727-733.
74. Lopez-Garcia P, Moreira D (1999) Metabolic symbiosis at the origin of eukaryotes. Trends Biochem Sci 24:88-93.
75. Mai Z, 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 19:2198-2205.
76. Marczak R, Gorrell TE, Muller M (1983) Hydrogenosomal ferredoxin of the anaerobic protozoon, Tritrichomonas foetus. J Biol Chem 258:12427-12433.
77. Martin W, Muller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37-41.
78. Marvin Sikkema FD, Pedro Gomes TM, Grivet JP, Gottschal JC, Prins RA (1993) Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch Microbiol 160:388-396.
79. McGoldrick JP, Yeh YC, Solomon M, Essigmann JM, Lu AL (1995) Characterization of a mammalian homolog of the Escherichia-coli Muty mismatch repair protein. Mol Cell Biol 15:989-996.
80. Moreira D, Lopez-Garcia P (1998) Symbiosis between methanogenic archaea and deltaproteobacteria as the origin of eukaryotes: The syntrophic hypothesis. J Mol Evol 47:517-530.
81. Muhlenhoff U, Lill R (2000) Biogenesis of iron-sulfur proteins in eukaryotes: A novel task of mitochondria that is inherited from bacteria. Biochim Biophys Acta 1459:370-382.
82. Muhlenhoff U, Gerber J, Richhardt N, Lill R (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J 22:4815-4825.
83. Muller M (1988) Energy metabolism of protozoa without mitochondria. Annu Rev Microbiol 42:465-488.
84. Muller M (2003). Energy metabolism. Part I: Anaerobic protozoa. In: Marr JJ, Nilsen TW, Komuniecki RW (eds) Molecular medical parasitology. Academic, New York, pp 125-139.
85. Nixon JEJ, Filed J, McArthur AG, Sogin ML, Yarlett N, Loftus BJ, Samuelson J (2003) Irondependent hydrogenases of Entamoeba histolytica and Giardia lamblia: Activity of the recombinant entamoebic enzyme and evidence for lateral gene transfer. Biol Bull 204:1-9.
86. Nixon JEJ, Wang A, Field J, Morrison HG, McArthur AG, Sogin ML, Loftus BJ, Samuelson J (2002a) Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryot Cell 1:181-190.
87. Paul RG, Williams AG, Butler RD (1990) Hydrogenosomes in the rumen entodiniomorphid ciliate Polyplastron multivesiculatum. J Gen Microbiol 136:1981-1989.
88. Payne MJ, Chapman A, Cammack R (1993) Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis. FEBS Lett 317:101-104.
89. Pilkington SJ, Skehel JM, Gennis RB, Walker JE (1991) Relationship between mitochondrial NADH-ubiquinone reductase and a bacterial NAD-reducing hydrogenase. Biochemistry 30:2166-2175.
90. Posewitz MC, King PW, Smolinski SL, Zhang LP, Seibert M, Ghirardi ML (2004) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711-25720.
91. Putignani L, Tait A, Smith HV, Horner D, Tovar J, Tetley L, Wastling JM (2004) Characterization of a mitochondrion-like organelle in Cryptosporidium parvum. Parasitol 129:1-18.
92. Putz S, Doležal P, Gelius-Dietrich G, Tachezy J, Henze K (2006) [Fe]-hydrogenase maturases in the hydrogenosomes of Trichomonas vaginalis. Eukaryot Cell 5:579-586.
93. 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.
94. Riordan CE, Langreth SG, Sanchez LB, Kayser O, Keithly JS (1999) Preliminary evidence for a mitochondrion in Cryptosporidium parvum: Phylogenetic and therapeutic implications. J Eukaryot Microbiol 46:52S-55S.
95. Riordan CE, Ault JG, Langreth SG, Keithly JS (2003) Cryptosporidium parvum Cpn60 targets a relict organelle. Curr Genet 44:138-147.
96. 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.
97. Roger AJ, Sandblom O, Doolittle WF, Philippe H (1999) An evaluation of elongation factor 1 alpha as a phylogenetic marker for eukaryotes. Mol Biol Evol 16:218-233.
98. Rotte C, Stejskal F, Zhu G, Keithly JS, 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.
99. Rouault TA, Tong WH (2005) Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol 6:345-351.
100. Roy A, Solodovnikova N, Nicholson T, Antholine W, Walden WE (2003) A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J 22:4826-4835.
101. Santos R, Buisson N, Knight SAB, Dancis A, Camadro JM, Lesuisse E (2004) Candida albicans lacking the frataxin homologue: A relevant yeast model for studying the role of frataxin. Mol Microbiol 54:507-519.
102. Schilke B, Voisine C, Beinert H, Craig E (1999) Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 96:10206-10211.
103. 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.
104. Simpson AGB, Patterson DJ (1999) The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the "excavate hypothesis". Eur J Protistol 35:353-370.
105. Simpson AGB, VandenHoff J, Bernard C, Burton HR, Patterson DJ (1997) The ultrastructure and systematic position of the euglenozoon Postgaardi mariagerensis, Fenchel et al. Arch Protist 147:213-225.
106. Sipos K, Lange H, Fekete Z, Ullmann P, Lill R, Kispal G (2002) Maturation of cytosolic ironsulfur proteins requires glutathione. J Biol Chem 277:26944-26949.
107. Šlapeta J, Keithly JS (2004) Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria. Eukaryot Cell 3:483-494.
108. Smith AD, Agar JN, Johnson KA, Frazzon J, Amster IJ, Dean DR, Johnson MK (2001) Sulfur transfer from IscS to IscU: The first step in iron-sulfur cluster biosynthesis. J Am Chem Soc 123:11103-11104.
109. Snyers L, Hellings P, Bovy-Kesler C, Thines-Sempoux D (1982) Occurence of hydrogenosomes in the rumen ciliates Ophryoscolecidae. FEBS Lett 137:35-39.
110. Steinbuchel A, Muller M (1986) Anaerobic pyruvate metabolism of Tritrichomonas foetus and Trichomonas vaginalis hydrogenosomes. Mol Biochem Parasitol 20:57-65.
111. Stejskal F, Šlapeta J, Čtrnacta V, Keithly JS (2003) A Narf-like gene from Cryptosporidium parvum resembles homologues observed in aerobic protists and higher eukaryotes. FEMS Microbiol Lett 229:91-96.
112. Suchan P, Vyoral D, Petrak J, Šut'ak R, Rasoloson D, Nohynkova E, Doležal P, Tachezy J (2003) Incorporation of iron into Tritrichomonas foetus cell compartments reveals ferredoxin as a major iron-binding protein in hydrogenosomes. Microbiology 149:1911-1921.
113. Šut'ak R, Doležal P, Fiumera HL, Hrdý I, Dancis A, Gadillo-Correa M, Johnson PJ, 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.
114. Tachezy J, Sanchez LB, 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.
115. Takahashi Y, Tokumoto U (2002) A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. J Biol Chem 277:28380-28383.
116. Thong KW, Coombs GH (1987) Comparative study of ferredoxin-linked and oxygenmetabolizing enzymes of trichomonads. Comp Biochem Physiol B 87:637-641.
117. Tielens AGM, Rotte C, van Hellemond JJ, Martin W (2002) Mitochondria as we don't know them. Trends Biochem Sci 27:564-572.
118. Tokumoto U, Kitamura S, Fukuyama K, Takahashi Y (2004) Interchangeability and distinct properties of bacterial Fe-S cluster assembly systems: functional replacement of the isc and suf operons in Escherichia coli with the nifSU-like operon from Helicobacter pylori. J Biochem 136:199-209.
119. 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.
120. Tovar J, Leon-Avila G, Sanchez LB, Šut'ak R, Tachezy J, van der GM, Hernandez M, Muller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172-176.
121. Upcroft P, Upcroft JA (2001) Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin Microbiol Rev 14:150-164.
122. van den Berg WAM, Hagen WR, van Dongen WMAM (2000) The hybrid-cluster protein ('prismane protein') from Escherichia coli - characterization of the hybrid-cluster protein, redox properties of the [2Fe-2S] and [4Fe-2S-20] clusters and identification of an associated NADH oxidoreductase containing FAD and [2Fe-2S]. Eur J Biochem 267:666-676.
123. 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.
124. van der Giezen M, Leon-Avila G, Tovar J (2005) Characterization of chaperonin 10 (Cpn10) from the intestinal human pathogen Entamoeba histolytica. Microbiology 151:3107-3115.
125. van Weelden SW, van Hellemond JJ, Opperdoes FR, Tielens AG (2005) New functions for parts of the Krebs cycle in procyclic Trypanosoma brucei, a cycle not operating as a cycle. J Biol Chem 280:12451-12460.
126. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455-501.
127. Vollmer M, Thomsen N, Wiek S, Seeber F (2001) Apicomplexan parasites possess distinct nuclear-encoded, but apicoplast-localized, plant-type ferredoxin-NADP(?) reductase and ferredoxin. J Biol Chem 276:5483-5490.
128. Voncken FGJ, Boxma B, van Hoek AHAM, Akhmanova AS, Vogels GD, Huynen M, Veenhuis M, Hackstein JHP (2002) A hydrogenosomal [Fe]-hydrogenase from the anaerobic chytrid Neocallimastix sp L2. Gene 284:103-112.
129. Williams BAP, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865-869.
130. Xu P, Widmer G, Wang YP, Ozaki LS, Alves JM, Serrano MG, Puiu D, Manque P, Akiyoshi D, Mackey AJ, Pearson WR, Dear PH, Bankier AT, Peterson DL, Abrahamsen MS, Kapur V, Tzipori S, Buck GA (2004) The genome of Cryptosporidium hominis. Nature 431:1107-1112.
131. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443-4447.
132. Yano T (2002) The energy-transducing NADH:quinone oxidoreductase, complex I. Mol Asp Med 23:345-368.
133. Yarlett N, Hackstein JHP (2005) Hydrogenosomes: one organelle, multiple origins. BioScience 55:657-667.
134. Yarlett N, Hann AC, Lloyd D, Williams A (1981) Hydrogenosomes in the rumen protozoon Dasytricha ruminantium Schuberg. Biochem J 200:365-372.
135. Yarlett N, Hann AC, Lloyd D, Williams AG (1983) Hydrogenosomes in a mixed isolate of Isotricha prostoma and Isotricha intestinalis from ovine rumen contents. Comp Biochem Physiol B 74:357-364.
136. Yarlett N, Orpin CG, Munn EA, Yarlett NC, Greenwood CA (1986a) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236:729-739.
137. Yarlett N, Yarlett NC, Lloyd D (1986b) Ferredoxin-dependent reduction of nitroimidazole derivatives in drug-resistant and susceptible strains of Trichomonas vaginalis. Biochem Pharmacol 35:1703-1708.
138. Yarunin A, Panse VG, Petfalski E, Dez C, Tollervey D, Hurt EC (2005) Functional link between ribosome formation and biogenesis of iron-sulfur proteins. EMBO J 24:580-588.
139. Zheng L, Cash VL, Flint DH, Dean DR (1998) Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273: 13264-13272.