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Metabolism of Trichomonad Hydrogenosomes

  • Ivan HrdýEmail author
  • Jan Tachezy
  • Miklós Müller
Chapter
  • 287 Downloads
Part of the Microbiology Monographs book series (MICROMONO, volume 9)

Abstract

Trichomonad hydrogenosomes are the best studied organelles of their kind to date. Their role in energy metabolism, antioxidant defense, and the assembly of iron-sulfur centers, the vital cofactors of a number of essential proteins, has been reliably established. In this chapter, we summarize our knowledge of trichomonad hydrogenosome biochemistry, particularly the energy-linked pathway, the oxygen- and reactive oxygen species-related biochemistry, and the iron-sulfur cluster assembly machinery. The structure of the proteins constituting the core pathway is dealt with in some detail. We also attempt to incorporate the results of the T. vaginalis genome annotation, proteomic, and biochemical studies into the metabolic scheme of the hydrogenosome.

Notes

Acknowledgments

The excellent technical assistance of Ms. Míša Marcinčiková is gratefully acknowledged.

Part of the original research presented in this chapter was supported by the NIH (grant no. AI 11942 to Miklós Müller), the Ministry of Education, Youth and Sports of the Czech Republic project NPU II (LQ1604), and by ERD Funds project CePaViP (CZ.02.1.01/0.0/0.0/16_019/0000759) to Jan Tachezy.

References

  1. Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65:125–153PubMedCrossRefGoogle Scholar
  2. Bauwe H, Kolukisaoglu U (2003) Genetic manipulation of glycine decarboxylation. J Exp Bot 54:1523–1535PubMedCrossRefGoogle Scholar
  3. Beltrán NC, Horváthová L, Jedelský PL et al (2013) Iron-induced changes in the proteome of Trichomonas vaginalis hydrogenosomes. PLoS One 8:e65148.  https://doi.org/10.1371/journal.pone.0065148 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Benchimol M, De Souza W (1983) Fine structure and cytochemistry of the hydrogenosome of Tritrichomonas foetus. J Protozool 30:422–425PubMedCrossRefGoogle Scholar
  5. Boxma B, de Graaf RM, van der Staay GWM et al (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434:74–79CrossRefGoogle Scholar
  6. Bui ET, Johnson PJ (1996) Identification and characterization of [Fe]-hydrogenases in the hydrogenosome of Trichomonas vaginalis. Mol Biochem Parasitol 76:305–310PubMedCrossRefGoogle Scholar
  7. Carlton JM, Hirt RP, Silva JC et al (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207–212PubMedPubMedCentralCrossRefGoogle Scholar
  8. Čerkasov J, Čerkasovová A, Kulda J, Vilhelmová D (1978) Respiration of hydrogenosomes of Tritrichomonas foetus. J Biol Chem 253:1207–1214Google Scholar
  9. Čerkasovová A, Čerkasov J, Kulda J, Reischig J (1976) Circular DNA and cardiolipin in hydrogenosomes, microbody-like organelles of trichomonads. Folia Parasitol Praha 23:33–37PubMedGoogle Scholar
  10. Chabrière E, Charon MH, Volbeda A et al (1999) Crystal structures of the key anaerobic enzyme pyruvate: ferredoxin oxidoreductase, free and in complex with pyruvate. Nat Struct Biol 6:182–190.  https://doi.org/10.1038/5870 CrossRefPubMedGoogle Scholar
  11. Chae HZ, Robison K, Poole LB et al (1994) Cloning and sequencing of thiol-specific antioxidant from mammalian brain – alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc Natl Acad Sci U S A 91:7017–7021PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chapman A, Linstead DJ, Lloyd D (1999) Hydrogen peroxide is a product of oxygen consumption by Trichomonas vaginalis. J Biosci 24:339–344CrossRefGoogle Scholar
  13. Chen KC, Amsel R, Eschenbach DA, Holmes KK (1982) Biochemical diagnosis of vaginitis: determination of diamines in vaginal fluid. J Infect Dis 145:337–345PubMedCrossRefGoogle Scholar
  14. Chen L, Liu MY, LeGall J et al (1993) Rubredoxin oxidase, a new flavo-hemo-protein, is the site of oxygen reduction to water by the strict anaerobe Desulfovibrio gigas. Biochem Biophys Res Commun 193:100–00105PubMedCrossRefGoogle Scholar
  15. Coombs GH, Westrop GD, Suchan P et al (2004) The amitochondriate eukaryote Trichomonas vaginalis contains a divergent t00hioredoxin-linked peroxiredoxin antioxidant system. J Biol Chem 279:5249–5256PubMedCrossRefPubMedCentralGoogle Scholar
  16. Crossnoe CR, Germanas JP, LeMagueres P et al (2002) The crystal structure of Trichomonas vaginalis ferredoxin provides insight into metronidazole activation. J Mol Biol 318:503–518PubMedCrossRefGoogle Scholar
  17. Cruz F, Ferry JG (2006) Interaction of iron-sulfur flavoprotein with oxygen and hydrogen peroxide. Biochim Biophys Acta – Gen Subj.  https://doi.org/10.1016/j.bbagen.2006.02.016 CrossRefGoogle Scholar
  18. Čtrnáctá V, Ault JG, Stejskal F, Keithly JS (2006) Localization of pyruvate: NADP(+) oxidoreductase in sporozoites of Cryptosporidium parvum. J Eukaryot Microbiol 53:225–231PubMedCrossRefGoogle Scholar
  19. Declerck PJ, Müller M (1987) Hydrogenosomal ATP: AMP phosphotransferase of Trichomonas vaginalis. Comp Biochem Physiol B 88:575–580.  https://doi.org/10.1016/0305-0491(87)90347-6 CrossRefPubMedGoogle Scholar
  20. Di Matteo A, Scandurra FM, Testa F et al (2008) The O2-scavenging flavodiiron protein in the human parasite Giardia intestinalis. J Biol Chem 283:4061–4068.  https://doi.org/10.1074/jbc.M705605200 CrossRefPubMedGoogle Scholar
  21. Docampo R, Moreno SN, Mason RP (1987) Free radical intermediates in the reaction of pyruvate: ferredoxin oxidoreductase in Tritrichomonas foetus hydrogenosomes. J Biol Chem 262:12417–12420PubMedGoogle Scholar
  22. Doležal P, Vaňáčová Š, Tachezy J et al (2004) Malic enzymes of Trichomonas vaginalis: two enzyme families, two distinct origins. Gene 329:81–92.  https://doi.org/10.1016/j.gene.2003.12.022 CrossRefPubMedGoogle Scholar
  23. Doležal P, Dancis A, Lesuisse E et al (2007) Frataxin, a conserved mitochondrial protein, in the hydrogenosome of Trichomonas vaginalis. Eukaryot Cell 6:1431–1438.  https://doi.org/10.1128/EC.00027-07 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Drmota T, Proost P, Van Ranst M et al (1996) Iron-ascorbate cleavable malic enzyme from hydrogenosomes of Trichomonas vaginalis: purification and characterization. Mol Biochem Parasitol 83:221–234PubMedCrossRefPubMedCentralGoogle Scholar
  25. Dyall SD, Yan W, Gadillo-Correa MG et al (2004) Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431:1103–1107PubMedCrossRefGoogle Scholar
  26. Ellis JE, Setchell KDR, Kaneshiro ES (1994a) Detection of ubiquinone in parasitic and free-living protozoa, including species devoid of mitochondria. Mol Biochem Parasitol 65:213–224PubMedCrossRefGoogle Scholar
  27. Ellis JE, Yarlett N, Cole D et al (1994b) Antioxidant defences in the microaerophilic protozoan Trichomonas vaginalis: comparison of metronidazole-resistant and sensitive strains. Microbiology 140:2489–2494.  https://doi.org/10.1099/13500872-140-9-2489 CrossRefPubMedGoogle Scholar
  28. Folgosa F, Martins MC, Teixeira M (2018) Diversity and complexity of flavodiiron NO/O2 reductases. FEMS Microbiol Lett 365.  https://doi.org/10.1093/femsle/fnx267
  29. Gabaldon T, Rainey D, Huynen MA (2005) Tracing the evolution of a large protein complex in the eukaryotes, NADH: ubiquinone oxidoreductase (Complex I). J Mol Biol 348:857–870PubMedCrossRefPubMedCentralGoogle Scholar
  30. Gakh O, Adamec J, Gacy AM et al (2002) Physical evidence that yeast frataxin is an iron storage protein. Biochemistry 41:6798–6804.  https://doi.org/10.1021/bi025566+ CrossRefPubMedGoogle Scholar
  31. Gomes CM, Giuffre A, Forte E et al (2002) A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin 2. J Biol Chem 277:25273–25276PubMedCrossRefGoogle Scholar
  32. Gorrell TE, Yarlett N, Müller M (1984) Isolation and characterization of Trichomonas vaginalis ferredoxin. Carlsberg Res Commun 246:529–536.  https://doi.org/10.1007/BF02913954 CrossRefGoogle Scholar
  33. Guschina IA, Harris KM, Maskrey B et al (2009) The microaerophilic flagellate, Trichomonas vaginalis, contains unusual acyl lipids but no detectable cardiolipin. J Eukaryot Microbiol 56:52–57PubMedCrossRefGoogle Scholar
  34. Gutierrez C, Devedjian JC (1991) Osmotic induction of gene osmC expression in Escherichia coli K12. J Mol Biol 220:959–973.  https://doi.org/10.1016/0022-2836(91)90366-E CrossRefPubMedGoogle Scholar
  35. Horváthová L, Šafaříková L, Basler M et al (2012) Transcriptomic identification of iron-regulated and iron-independent gene copies within the heavily duplicated Trichomonas vaginalis genome. Genome Biol Evol 4:1017–1029.  https://doi.org/10.1093/gbe/evs078 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hrdý I, Müller M (1995) Primary structure and eubacterial relationships of the pyruvate:Ferredoxin oxidoreductase of the amitochondriate eukaryote Trichomonas vaginalis. J Mol Evol 41:388–396.  https://doi.org/10.1007/BF00186551 CrossRefPubMedGoogle Scholar
  37. Hrdý I, Mertens E, Van Schaftingen E (1993) Identification, purification and separation of different isozymes of NADP-specific malic enzyme from Tritrichomonas foetus. Mol Biochem Parasitol 57:253–260PubMedCrossRefGoogle Scholar
  38. Hrdý I, Hirt RP, Doležal P et al (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618–622PubMedCrossRefGoogle Scholar
  39. Hrdý I, Cammack R, Stopka P et al (2005) Alternative pathway of metronidazole activation in Trichomonas vaginalis hydrogenosomes. Antimicrob Agents Chemother 49:5033–5036.  https://doi.org/10.1128/AAC.49.12.5033-5036.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Huang KY, Ku FM, Cheng WH et al (2015) Novel insights into the molecular events linking to cell death induced by tetracycline in the amitochondriate protozoan Trichomonas vaginalis. Antimicrob Agents Chemother 59:6891–6903.  https://doi.org/10.1128/AAC.01779-15 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Huber M, Garfinkel L, Gitler C et al (1988) Nucleotide-sequence analysis of an Entamoeba histolytica ferredoxin gene. Mol Biochem Parasitol 31:27–33PubMedCrossRefGoogle Scholar
  42. Hug LA, Stechmann A, Roger AJ (2010) Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol Biol Evol 27:311–324.  https://doi.org/10.1093/molbev/msp237 CrossRefPubMedGoogle Scholar
  43. Igarashi K, Kashiwagi K (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271:559–564PubMedCrossRefGoogle Scholar
  44. Inui H, Ono K, Miyatake K et al (1987) Purification and characterization of pyruvate - NADP+ oxidoreductase in Euglena gracilis. J Biol Chem 262:9130–9135PubMedPubMedCentralGoogle Scholar
  45. Janssen BD, Chen YP, Molgora BM et al (2018) CRISPR/Cas9-mediated gene modification and gene knock out in the human-infective parasite Trichomonas vaginalis. Sci Rep 8:270.  https://doi.org/10.1038/s41598-017-18442-3 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Jenkins TM, Gorrell TE, Müller M, Weitzman PD (1991) Hydrogenosomal succinate thiokinase in Tritrichomonas foetus and Trichomonas vaginalis. Biochem Biophys Res Commun 179:892–896PubMedCrossRefGoogle Scholar
  47. Jin S, Kurtz DM, Liu ZJ et al (2002) X-ray crystal structures of reduced rubrerythrin and its azide adduct: a structure-based mechanism for a non-heme diiron peroxidase. J Am Chem Soc 124:9845–9855PubMedCrossRefGoogle Scholar
  48. Johnson D, Dean D (2004) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74:247–281CrossRefGoogle Scholar
  49. Johnson PJ, d’Oliveira CE, Gorrell TE et al (1990) Molecular analysis of the hydrogenosomal ferredoxin of the anaerobic protist Trichomonas vaginalis. Proc Natl Acad Sci U S A 87:6097–6101.  https://doi.org/10.1073/pnas.87.16.6097 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kulda J (1999) Trichomonads, hydrogenosomes and drug resistance. Int J Parasitol 29:199–212PubMedCrossRefGoogle Scholar
  51. Lahti CJ, d’Oliveira CE, Johnson PJ (1992) Beta-succinyl-coenzyme A synthetase from Trichomonas vaginalis is a soluble hydrogenosomal protein with an amino-terminal sequence that resembles mitochondrial presequences. J Bacteriol 174:6822–6830PubMedPubMedCentralCrossRefGoogle Scholar
  52. Lahti CJ, Bradley PJ, Johnson PJ (1994) Molecular characterization of the alpha-subunit of Trichomonas vaginalis hydrogenosomal succinyl CoA synthetase. Mol Biochem Parasitol 66:309–318PubMedCrossRefGoogle Scholar
  53. Land KM, Delgadillo-Correa MG, Tachezy J et al (2004) Targeted gene replacement of a ferredoxin gene in Trichomonas vaginalis does not lead to metronidazole resistance. Mol Microbiol 51:115–122PubMedCrossRefGoogle Scholar
  54. Lange S, Rozario C, Müller M (1994) Primary structure of the hydrogenosomal adenylate kinase of Trichomonas vaginalis and its phylogenetic relationships. Mol Biochem Parasitol 66:297–308PubMedCrossRefGoogle Scholar
  55. Lantsman Y, Tan KSW, Morada M, Yarlett N (2008) Biochemical characterization of amitochondrial-like organelle from Blastocystis sp. subtype 7. Microbiology 154(Pt 9):2757–2766.  https://doi.org/10.1099/mic.0.2008/017897-0 CrossRefGoogle Scholar
  56. Leger MM, Gawryluk RMR, Gray MW, Roger AJ (2013) Evidence for a hydrogenosomal-type anaerobic ATP generation pathway in Acanthamoeba castellanii. PLoS One 8:e69532.  https://doi.org/10.1371/journal.pone.0069532 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Leger MM, Eme L, Hug LA, Roger AJ (2016) Novel hydrogenosomes in the microaerophilic jakobid Stygiella incarcerata. Mol Biol Evol 33:2318–2336.  https://doi.org/10.1093/molbev/msw103 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Leitsch D (2017) A review on metronidazole: an old warhorse in antimicrobial chemotherapy. Parasitology 23:1–12.  https://doi.org/10.1017/S0031182017002025 CrossRefGoogle Scholar
  59. Leitsch D, Kolarich D, Binder M et al (2009) Trichomonas vaginalis: metronidazole and other nitroimidazole drugs are reduced by the flavin enzyme thioredoxin reductase and disrupt the cellular redox system. Implications for nitroimidazole toxicity and resistance. Mol Microbiol 72:518–536.  https://doi.org/10.1111/j.1365-2958.2009.06675.x CrossRefPubMedGoogle Scholar
  60. Leitsch D, Janssen BD, Kolarich D et al (2014) Trichomonas vaginalis flavin reductase 1 and its role in metronidazole resistance. Mol Microbiol 91:198–208.  https://doi.org/10.1111/mmi.12455 CrossRefPubMedGoogle Scholar
  61. Leitsch D, Williams CF, Hrdý I (2018) Redox pathways as drug targets in microaerophilic parasites. Trends Parasitol 34:576–589PubMedCrossRefPubMedCentralGoogle Scholar
  62. Lill R, Kispal G (2000) Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem Sci 25:352–356PubMedCrossRefGoogle Scholar
  63. Lill R, Mühlenhoff U (2006) Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu Rev Cell Dev Biol 22:457–486PubMedCrossRefGoogle Scholar
  64. Lill R, Dutkiewicz R, Freibert SA et al (2015) The role of mitochondria and the CIA machinery in the maturation of cytosolic and nuclear iron-sulfur proteins. Eur J Cell Biol 94:280–291PubMedCrossRefGoogle Scholar
  65. Lindmark DG (1976) Acetate production by Tritrichomonas foetus. In: Van den Bossche H (ed) Biochemistry of parasites and host-parasite relationships. Elsevier, Amsterdam, pp 15–21Google Scholar
  66. Lindmark DG, Müller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 248:7724–7728Google Scholar
  67. Lindmark DG, Müller M (1974) Superoxide dismutase in the anaerobic flagellates, Tritrichomonas foetus and Monocercomonas sp. J Biol Chem 249:4634–4637PubMedGoogle Scholar
  68. Lindmark DG, Müller M, Shio H (1975) Hydrogenosomes in Trichomonas vaginalis. J Parasitol 61:552–554CrossRefGoogle Scholar
  69. Linstead DJ, Bradley S (1988) The purification and properties of two soluble reduced nicotinamide: acceptor oxidoreductases from Trichomonas vaginalis. Mol Biochem Parasitol 27:125–133PubMedCrossRefGoogle Scholar
  70. Lloyd D, Kristensen B (1985) Metronidazole inhibition of hydrogen production in vivo in drug-sensitive and resistant strains of Trichomonas vaginalis. J Gen Microbiol 131:849–853PubMedGoogle Scholar
  71. Long S, Jirků M, Mach J, Ginger M, Šuťák R, Richardson DR, Tachezy J, Lukeš J (2008) Ancestral roles of eukaryotic frataxin: mitochondrial frataxin function and heterologous expression of hydrogenosomal Trichomonas homologues in trypanosomes. Mol Microbiol 69:94–109PubMedCrossRefGoogle Scholar
  72. Mallo N, Lamas J, Leiro JM (2013) Hydrogenosome metabolism is the key target for antiparasitic activity of resveratrol against Trichomonas vaginalis. Antimicrob Agents Chemother 57:2476–2484.  https://doi.org/10.1128/AAC.00009-13 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Marczak R, Gorrell TE, Müller M (1983) Hydrogenosomal ferredoxin of the anaerobic protozoon, Tritrichomonas foetus. J Biol Chem 258:12427–12433PubMedGoogle Scholar
  74. McGonigle S, Dalton JP, James ER (1998) Peroxidoxins: a new antioxidant family. Parasitol Today 14:139–145PubMedCrossRefGoogle Scholar
  75. Mentel M, Zimorski V, Haferkamp P et al (2008) Protein import into hydrogenosomes of Trichomonas vaginalis involves both N-terminal and internal targeting signals: a case study of thioredoxin reductases. Eukaryot Cell 7:1750–1757.  https://doi.org/10.1128/EC.00206-08 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Mertens E, Van Schaftingen E, Müller M (1992) Pyruvate kinase from Trichomonas vaginalis, an allosteric enzyme stimulated by ribose 5-phosphate and glycerate 3-phosphate. Mol Biochem Parasitol 54:13–20PubMedCrossRefGoogle Scholar
  77. Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64:1063–1084PubMedCrossRefGoogle Scholar
  78. Mogi T, Kita K (2010) Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium. Parasitol Int 59:305–312PubMedCrossRefGoogle Scholar
  79. Mongkolsuk S, Praituan W, Loprasert S et al (1998) Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J Bacteriol 180:2636–2643PubMedPubMedCentralGoogle Scholar
  80. Morada M, Smid O, Hampl V et al (2011) Hydrogenosome-localization of arginine deiminase in Trichomonas vaginalis. Mol Biochem Parasitol 176:51–54.  https://doi.org/10.1016/j.molbiopara.2010.10.004 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Mukherjee M, Brown MT, McArthur AG, Johnson PJ (2006a) Proteins of the glycine decarboxylase complex in the hydrogenosome of Trichomonas vaginalis. Eukaryot Cell 5:2062–2071PubMedPubMedCentralCrossRefGoogle Scholar
  82. Mukherjee M, Sievers SA, Brown MT, Johnson PJ (2006b) Identification and biochemical characterization of serine hydroxymethyl transferase in the hydrogenosome of Trichomonas vaginalis. Eukaryot Cell 5:2072–2078PubMedPubMedCentralCrossRefGoogle Scholar
  83. Müller M (1993) The hydrogenosome. J Gen Microbiol 139:2879–2889.  https://doi.org/10.1099/00221287-139-12-2879 CrossRefGoogle Scholar
  84. Müller M, Lindmark DG (1978) Respiration of hydrogenosomes of Tritrichomonas foetus. II. Effect of CoA on pyruvate oxidation. J Biol Chem 253:1215–1218PubMedGoogle Scholar
  85. Müller S, Liebau E, Walter RD, Krauth-Siegel RL (2003) Thiol-based redox metabolism of protozoan parasites. Trends Parasitol 19:320–328PubMedCrossRefGoogle Scholar
  86. Müller M, Mentel M, van Hellemond JJ et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495PubMedPubMedCentralCrossRefGoogle Scholar
  87. Novák L, Zubáčová Z, Karnkowska A et al (2016) Arginine deiminase pathway enzymes: evolutionary history in metamonads and other eukaryotes. BMC Evol Biol 16:197.  https://doi.org/10.1186/s12862-016-0771-4 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Nývltová E, Smutná T, Tachezy J, Hrdý I (2016) OsmC and incomplete glycine decarboxylase complex mediate reductive detoxification of peroxides in hydrogenosomes of Trichomonas vaginalis. Mol Biochem Parasitol 206:29–38PubMedCrossRefPubMedCentralGoogle Scholar
  89. Page-Sharp M, Behm CA, Smith GD et al (1996) Tritrichomonas foetus and Trichomonas vaginalis: the pattern of inactivation of hydrogenase activity by oxygen and activities of catalase and ascorbate peroxidase. Microbiology 142:207–211PubMedCrossRefGoogle Scholar
  90. Paget TA, Lloyd D (1990) Trichomonas vaginalis requires traces of oxygen and high concentrations of carbon dioxide for optimal growth. Mol Biochem Parasitol 41:65–72PubMedCrossRefGoogle Scholar
  91. Paltauf F, Meingassner JG (1982) The absence of cardiolipin in hydrogenosomes of Trichomonas vaginalis and Tritrichomonas foetus. J Parasitol 68:949–950PubMedCrossRefPubMedCentralGoogle Scholar
  92. Paul VD, Lill R (2015) Biogenesis of cytosolic and nuclear iron-sulfur proteins and their role in genome stability. Biochim Biophys Acta – Mol Cell Res 1853:1528–1539CrossRefGoogle Scholar
  93. Payne MJ, Chapman A, Cammack R (1993) Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis. FEBS Lett 317:101–104PubMedCrossRefPubMedCentralGoogle Scholar
  94. Pegg AE (1986) Recent advances in the biochemistry of polyamines in eukaryotes. Biochem J 234:249–262.  https://doi.org/10.1016/j.eswa.2016.05.028 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Peters JW, Schut GJ, Boyd ES et al (2015) [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochim Biophys Acta 1853:1350–1369.  https://doi.org/10.1016/j.bbamcr.2014.11.021 CrossRefGoogle Scholar
  96. Pütz S, Gelius-Dietrich G, Piotrowski M, Henze K (2005) Rubrerythrin and peroxiredoxin: two novel putative peroxidases in the hydrogenosomes of the microaerophilic protozoon Trichomonas vaginalis. Mol Biochem Parasitol 142:212–223PubMedCrossRefPubMedCentralGoogle Scholar
  97. Pütz S, Doležal P, Gelius-Dietrich G et al (2006) Fe-hydrogenase maturases in the hydrogenosomes of Trichomonas vaginalis. Eukaryot Cell 5:579–586PubMedPubMedCentralCrossRefGoogle Scholar
  98. Rada P, Doležal P, Jedelský PL et al (2011) The core components of organelle biogenesis and membrane transport in the hydrogenosomes of Trichomonas vaginalis. PLoS One 6:e24428.  https://doi.org/10.1371/journal.pone.0024428 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Rasoloson D, Vaňáčová Š, Tomková E et al (2002) Mechanisms of in vitro development of resistance to metronidazole in Trichomonas vaginalis. Microbiology 148:2467–2477.  https://doi.org/10.1099/00221287-148-8-2467 CrossRefPubMedGoogle Scholar
  100. Reeves PR, Guthrie JD, Lobelle-Rich P (1980) Entamoeba histolytica: isolation of ferredoxin. Exp Parasitol 49:83–88PubMedCrossRefPubMedCentralGoogle Scholar
  101. Reis IA, Martinez MP, Yarlett N et al (1999) Inhibition of polyamine synthesis arrests trichomonad growth and induces destruction of hydrogenosomes. Antimicrob Agents Chemother 43:1919–1923PubMedPubMedCentralCrossRefGoogle Scholar
  102. Rivière L, Van Weelden SWH, Glass P et al (2004) Acetyl:succinate CoA-transferase in procyclic Trypanosoma brucei. Gene identification and role in carbohydrate metabolism. J Biol Chem.  https://doi.org/10.1074/jbc.M407513200 PubMedCrossRefGoogle Scholar
  103. Rotte C, Stejskal F, Zhu G et al (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 18:710–720PubMedCrossRefGoogle Scholar
  104. Rubach JK, Brazzolotto X, Gaillard J, Fontecave M (2005) Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima. FEBS Lett 579:5055–5060PubMedCrossRefGoogle Scholar
  105. Santos R, Buisson N, Knight SAB et al (2004) Candida albicans lacking the frataxin homologue: a relevant yeast model for studying the role of frataxin. Mol Microbiol 54:507–519.  https://doi.org/10.1111/j.1365-2958.2004.04281.x CrossRefPubMedGoogle Scholar
  106. Schirch V, Szebenyi DME (2005) Serine hydroxymethyltransferase revisited. Curr Opin Chem Biol 9:482–487.  https://doi.org/10.1016/j.cbpa.2005.08.017 CrossRefPubMedPubMedCentralGoogle Scholar
  107. Schneider RE, Brown MT, Shiflett AM et al (2011) The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int J Parasitol 41:1421–1434PubMedPubMedCentralCrossRefGoogle Scholar
  108. Schut GJ, Adams MWW (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191:4451–4457.  https://doi.org/10.1128/JB.01582-08 CrossRefPubMedPubMedCentralGoogle Scholar
  109. Slamovits CH, Keeling PJ (2006) Pyruvate-phosphate dikinase of oxymonads and parabasalia and the evolution of pyrophosphate-dependent glycolysis in anaerobic eukaryotes. Eukaryot Cell 5:148–154PubMedPubMedCentralCrossRefGoogle Scholar
  110. Smutná T, Goncalves VL, Saraiva LM et al (2009) Flavodiiron protein from Trichomonas vaginalis hydrogenosomes: the terminal oxygen reductase. Eukaryot Cell 8:47–55PubMedCrossRefGoogle Scholar
  111. Smutná T, Pilařová K, Tarábek J et al (2014) Novel functions of an iron-sulfur flavoprotein from Trichomonas vaginalis hydrogenosomes. Antimicrob Agents Chemother 58:3224–3232PubMedPubMedCentralCrossRefGoogle Scholar
  112. Stairs CW, Eme L, Brown MW et al (2014) A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia. Curr Biol 24:1176–1186.  https://doi.org/10.1016/j.cub.2014.04.033 CrossRefPubMedGoogle Scholar
  113. Stehling O, Wilbrecht C, Lill R (2014) Mitochondrial iron-sulfur protein biogenesis and human disease. Biochimie 100:61–77PubMedCrossRefGoogle Scholar
  114. Steinbüchel A, Müller M (1986) Anaerobic pyruvate metabolism of Tritrichomonas foetus and Trichomonas vaginalis hydrogenosomes. Mol Biochem Parasitol 20:57–65PubMedCrossRefGoogle Scholar
  115. Sutak R, Doležal P, Fiumera HL et al (2004) Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc Natl Acad Sci U S A 101:10368–10373PubMedPubMedCentralCrossRefGoogle Scholar
  116. Sutak R, Hrdý I, Doležal P et al (2012) Secondary alcohol dehydrogenase catalyzes the reduction of exogenous acetone to 2-propanol in Trichomonas vaginalis. FEBS J 279:2768–2780PubMedCrossRefGoogle Scholar
  117. Tabor CW, Tabor H (1976) 1,4-Diaminobutane (Putrescine), Spermidine, and Spermine. Annu Rev Biochem 45:285–306PubMedCrossRefGoogle Scholar
  118. Tachezy J, Sanchez LB, Müller 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 18:1919–1928PubMedCrossRefGoogle Scholar
  119. Tadolini B (1988) Polyamine inhibition of lipoperoxidation – the influence of polyamines on iron oxidation in the presence of compounds mimicking phospholipid polar heads. Biochem J 249:33–36PubMedPubMedCentralCrossRefGoogle Scholar
  120. Tanabe M (1979) Trichomonas vaginalis NADH oxidase activity. Exp Parasitol 48:135–143PubMedCrossRefGoogle Scholar
  121. Thong KW, Coombs GH (1987) Trichomonas species: homocysteine desulphurase and serine sulphydrase activities. Exp Parasitol 63:143–151PubMedCrossRefGoogle Scholar
  122. Townson M, Hanson GR, Upcroft JA, Upcroft P (1994) Purified ferredoxin from Giardia duodenalis. Eur J Biochem 220:439–446PubMedCrossRefGoogle Scholar
  123. van Grinsven KWA, Rosnowsky S, Van Weelden SWH et al (2008) Acetate:succinate CoA-transferase in the hydrogenosomes of Trichomonas vaginalis: Identification and characterization. J Biol Chem 283:1411–1418.  https://doi.org/10.1074/jbc.M702528200 CrossRefPubMedGoogle Scholar
  124. van Grinsven KWA, van Hellemond JJ, Tielens AGM (2009) Acetate:succinate CoA-transferase in the anaerobic mitochondria of Fasciola hepatica. Mol Biochem Parasitol 164:74–79.  https://doi.org/10.1016/j.molbiopara.2008.11.008 CrossRefPubMedGoogle Scholar
  125. Vicente JB, Tran V, Pinto L et al (2012) A detoxifying oxygen reductase in the anaerobic protozoan Entamoeba histolytica. Eukaryot Cell 11:1112–1118.  https://doi.org/10.1128/EC.00149-12 CrossRefPubMedPubMedCentralGoogle Scholar
  126. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501PubMedCrossRefGoogle Scholar
  127. Vilela R, Menna-Barreto RFS, Benchimol M (2010) Methyl jasmonate induces cell death and loss of hydrogenosomal membrane potential in Trichomonas vaginalis. Parasitol Int 59:387–393.  https://doi.org/10.1016/j.parint.2010.05.003 CrossRefPubMedGoogle Scholar
  128. Viscogliosi E, Delgado-Viscogliosi P, Gerbod D et al (1998) Cloning and expression of an iron-containing superoxide dismutase in the parasitic protist, Trichomonas vaginalis. FEMS Microbiol Lett 161:115–123PubMedCrossRefPubMedCentralGoogle Scholar
  129. Westrop GD, Wang L, Blackburn GJ et al (2017) Metabolomic profiling and stable isotope labelling of Trichomonas vaginalis and Tritrichomonas foetus reveal major differences in amino acid metabolism including the production of 2-hydroxyisocaproic acid, cystathionine and S-methylcysteine. PLoS One 12:e0189072.  https://doi.org/10.1371/journal.pone.0189072 CrossRefPubMedPubMedCentralGoogle Scholar
  130. Williams K, Lowe PN, Leadlay PF (1987) Purification and characterization of pyruvate: ferredoxin oxidoreductase from the anaerobic protozoon Trichomonas vaginalis. Biochem J 246:529–536PubMedPubMedCentralCrossRefGoogle Scholar
  131. Wood ZA, Schroder E, Harris JR, Poole LB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:32–40PubMedCrossRefGoogle Scholar
  132. Yarlett N, Lindmark DG, Goldberg B et al (1994) Subcellular localization of the enzymes of the arginine dihydrolase pathway in Trichomonas vaginalis and Tritrichomonas foetus. J Eukaryot Microbiol 41:554–559PubMedCrossRefGoogle Scholar
  133. Yarlett N, Martinez MP, Moharrami MA, Tachezy J (1996) The contribution of the arginine dihydrolase pathway to energy metabolism by Trichomonas vaginalis. Mol Biochem Parasitol 78:117–125PubMedCrossRefGoogle Scholar
  134. Zhao T, Cruz F, Ferry JG (2001) Iron-sulfur flavoprotein (Isf) from Methanosarcina thermophila is the prototype of a widely distributed family. J Bacteriol 183:6225–6233PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Faculty of Science, Department of Parasitology, BIOCEVCharles UniversityVestecCzech Republic
  2. 2.The Rockefeller UniversityNew YorkUSA

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