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Anaerobic Eukaryotes in Pursuit of Phylogenetic Normality: the Evolution of Hydrogenosomes and Mitosomes

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Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes

Part of the book series: Microbiology Monographs ((MICROMONO,volume 9))

Abstract

The evolutionary relationship of hydrogenosomes and mitosomes to mitochondria is no longer an issue of contention for specialists who work on the organelles. Hydrogenosomes and mitosomes are mitochondria in the evolutionary sense in that they descend from one and the same eubacterial endosymbiont, but the evolutionary significance of eukaryotic anaerobes that possess hydrogenosomes, mitosomes, and anaerobically functioning mitochondria is an issue of some contention. This chapter serves to further develop the thesis that the role of oxygen in eukaryote evolution needs to be reconsidered and viewed in light of what geologists have discovered relatively recently regarding oxygen in Earth history. According to newer findings from geochemical studies, there existed during a protracted period of Earth ocean history, during which the oceans were mostly anoxic and sulfidic (“Canfield” oceans). This period started about 2.3 billion years ago and only came to an end about 580 million years ago. This was the time during which eukaryotes arose and diversified into their major lineages. In light of this, anaerobic eukaryotes with mitochondria are not, in an evolutionary sense, strange, obscure, unexpected, or otherwise out of the ordinary, hence no special or unusual mechanisms are required to explain their origin. They are normal in every respect, and so are their mitochondria.

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References

  • Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Euk Microbiol 52:399–451

    PubMed  Google Scholar 

  • Allen CA, Van der Giezen M, Allen JF (2007) Origin, function, and transmission of mitochondria. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 39–56

    Google Scholar 

  • Anbar AD, Knoll AH (2002) Proterozoic ocean chemistry and evolution: A bioinorganic bridge. Science 297:1137–1142

    PubMed  CAS  Google Scholar 

  • Andersson JO, Sjogren AM, Horner DS, Murphy CA, Dyal PL, Svard SG, Logsdon JM, Ragan MA, Hirt RP, Roger AJ (2007) A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC GENOMICS 8:Art No 51

    Google Scholar 

  • Andersson SGE, Karlberg O, Canback B, Kurland CG (2003) On the origin of mitochondria: a genomics perspective. Phil Trans Roy Soc Lond B 358:165–177

    CAS  Google Scholar 

  • Andersson SGE, Kurland CG (1999) Origins of mitochondria and hydrogenosomes. Curr Opin Microbiol 2:535–541

    PubMed  CAS  Google Scholar 

  • Arnold GL, Anbar AD, Barling J, Lyons TW (2004) Molybdenum isotope evidence for widespread anoxia in mid-Proterozoic oceans. Science 304:87–90

    PubMed  CAS  Google Scholar 

  • Atteia A, van Lis R, Mendoza-Hernández G, Henze K, Martin W, Riveros-Rosas H, González-Halphen D (2003) Bifunctional aldehyde/alcohol dehydrogenase (ADHE) in chlorophyte algal mitochondria. Plant Mol Biol 53:175–188

    PubMed  CAS  Google Scholar 

  • Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate : formate lyase and a novel route of eukaryotic ATP-synthesis in anaerobic Chlamydomonas mitochondria. J Biol Chem 281:9909–9918

    PubMed  CAS  Google Scholar 

  • Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972–977

    PubMed  CAS  Google Scholar 

  • Barberà MJ, Ruiz-Trillo I, Leigh J, Hug LA, Roger AJ (2007) The diversity of mitochondrion-related organelles amongst eukaryotic microbes. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 239–276

    Google Scholar 

  • Benton MJ, Donoghue PC (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53

    PubMed  CAS  Google Scholar 

  • Bernhard JM, Buck KR, Farmer MA, Bowser SS (2000) The Santa Barbara basin is a symbiosis oasis. Nature 403:77–80

    PubMed  CAS  Google Scholar 

  • Biagini GA, van der Giezen M, Hill B, Winters C, Lloyd D (1994) Ca2+-accumulation in the hydrogenosome of Neocallimastix frontalis: a mitochondrial-like physiological role. FEMS Microbiol Lett 149:227–232

    Google Scholar 

  • Biagini GA, Finlay BJ, Lloyd D (1997) The evolution of the hydrogenosome. FEMS Microbiol Lett 155:133–140

    PubMed  CAS  Google Scholar 

  • Boxma B, de Graaf RM, van der Staay GW, van Alen TA, Ricard G, Gabaldon T, van Hoek AH, Moon-van der Staay SY, Koopman WJ, van Hellemond JJ, Tielens AG, Friedrich T, Veenhuis M, Huynen MA, Hackstein JH (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434:74–79

    PubMed  CAS  Google Scholar 

  • 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 spE2 produces ethanol via pyruvate : formate lyase and an alcohol dehydrogenase E. Mol Microbiol 51:1389–1399

    PubMed  CAS  Google Scholar 

  • Brocks JJ, Love GD, Summons RE, Knoll AH, Logan GA, Bowden SA (2005) Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea. Nature 437:866–870

    PubMed  CAS  Google Scholar 

  • Brondijk THC, Durand R, van der Giezen M, Gottschal JC, Prins RA, Fevre M (1996) scsB, a cDNA encoding the hydrogenosomal beta subunit of succinyl-CoA synthetase from the anaerobic fungus Neocallimastix frontalis. Mol Gen Genet 253:315–323

    PubMed  CAS  Google Scholar 

  • Canfield DE, Poulton SW, Narbonne GM (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95

    PubMed  CAS  Google Scholar 

  • Canfield DE (1998) A new model for Proterozoic ocean chemistry. Nature 396:450–453

    CAS  Google Scholar 

  • Canfield DE, Habicht KS, Thamdrup B (2000) The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288:658–661

    PubMed  CAS  Google Scholar 

  • Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UCM, Besteiro S, Sicheritz-Ponten T, Noel CJ, Dacks JB, Foster PG, Simillion C, Van de Peer Y, Miranda-Saavedra D, Barton GJ, Westrop GD, Müller S, Dessi D, Fiori PL, Ren Q, Paulsen I, Zhang H, Bastida-Corcuera FD, Simoes-Barbosa A, Brown MT, Hayes RD, Mukherjee M, Okumura CY, Schneider R, Smith AJ, Vanacova S, Villalvazo M, Haas BJ, Pertea M, Feldblyum TV, Utterback TR, Shu C-L, Osoegawa K, de Jong PJ, Hrdy I, Horvathova L, Zubacova Z, Dolezal P, Malik S-B, Logsdon JM, Henze K, Gupta A, Wang CC, Dunne RL, Upcroft JA, Upcroft P, White O, Salzberg SL, Tang P, Chiu C-H, Lee Y-S, Embley TM, Coombs GH, Mottram JC, Tachezy J, Fraser-Liggett CM, Johnson PJ (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207–212

    PubMed  Google Scholar 

  • Cavalier-Smith T (1975) The origin of nuclei and of eukaryotic cells. Nature 256:463–468

    Google Scholar 

  • Cavalier-Smith T (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354

    PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2004) Only six kingdoms of life. Proc Roy Soc Lond B 271:1251–1262

    CAS  Google Scholar 

  • Cavalier-Smith T (2007) The chimaeric origin of mitochondria: Photosynthetic cell enslavement, gene-transfer pressure, and compartmentation efficiency. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 161–200

    Google Scholar 

  • Cloud PE (1968) Atmospheric and hydrospheric evolution on the primitive Earth. Science 160:729–736

    PubMed  CAS  Google Scholar 

  • Dacks JB, Dyal PL, Embley TM, van der Giezen M (2006) Hydrogenosomal succinyl-CoA synthetase from the rumen-dwelling fungus Neocallimastix patriciarum; an energy-producing enzyme of mitochondrial origin. Gene 373:75–82

    PubMed  CAS  Google Scholar 

  • Davidov Y, Jurkevitch E (2007) Comments of Poole and Penny's essay Evaluating hypotheses for the orign of eukaryotes. BioEssays 29:615–616

    PubMed  Google Scholar 

  • de Duve C (2007) The origin of eukaryotes: A reappraisal. Nat Rev Genet 8:395–403

    PubMed  Google Scholar 

  • de Duve C (1969) Evolution of the peroxisome. Ann NY Acad Sci 168:369–381

    PubMed  Google Scholar 

  • de Zwaan A (1991) Molluscs. In: Bryant C (ed) Metazoan Life Without Oxygen. Chapman and Hall, London, pp 186–217

    Google Scholar 

  • Dietrich LEP, Tice MM, Newmann DK (2006) The co-evolution of life and Earth. Curr Biol 16:R395–R400

    PubMed  CAS  Google Scholar 

  • Doeller JE, Grieshaber MK, Kraus DW (2001) Chemolithoheterotrophy in a metazoan tissue: thiosulfate production matches ATP demand in ciliated mussel gills. J Exp Biol 204:3755–3764

    PubMed  CAS  Google Scholar 

  • Dolezal P, Likic V, Tachezy J, Lithgow T (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313:314–318

    PubMed  CAS  Google Scholar 

  • Doolittle WF (1980) Revolutionary concepts in evolutionary cell biology. Trends Biochem Sci 5:146–149

    CAS  Google Scholar 

  • Doolittle WF (1998) A paradigm gets shifty. Nature 392:15–16

    PubMed  CAS  Google Scholar 

  • Dyall SD, Yan WH, Delgadillo-Correa MG, Lunceford A, Loo JA, Clarke CF, Johnson PJ (2004) Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431:1103–1107

    PubMed  CAS  Google Scholar 

  • Ellis JE, Lindmark DG, Williams AG, Lloyd D (1994) Polypeptides of hydrogenosome-enriched fractions from rumen ciliate protozoa and trichomonads: immunological studies. FEMS Microbiol Lett 117:211–216

    PubMed  CAS  Google Scholar 

  • Embley TM, Finlay BJ, Dyal PL, Hirt RP, Wilkinson M, Williams AG (1995) Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc R Soc Lond B 262:87–93

    CAS  Google Scholar 

  • Embley TM, Horner DA, Hirt RP (1997) Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria? Trends Ecol Evol 12:437–441

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630

    PubMed  CAS  Google Scholar 

  • Emelyanov VV (2007) Constantin Merezhkowsky and the endokaryotic hypothesis. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 201–238

    Google Scholar 

  • Fenchel TM, Riedl RJ (1970) The sulfide system: A new biotic community underneath the oxidized layer of marine sand bottoms. Marine Biol 7:255–268

    CAS  Google Scholar 

  • Fike DA, Grotzinger JP, Pratt LM, Summons RE (2006) Oxidation of the Ediacaran ocean. Nature 444:744–747

    PubMed  CAS  Google Scholar 

  • Gabaldon T, Snel B, van Zimmeren F, Hemrika W, Tabak H, Huynen MA (2006) Origin and evolution of the peroxisomal proteome. Biol Direct 1:8

    PubMed  Google Scholar 

  • 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 Euk Microbiol 51:456–463

    PubMed  CAS  Google Scholar 

  • Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Ann Rev Physiol 60:30–53

    Article  Google Scholar 

  • Grieshaber M, Hardewig I, Kreutzer U, Pörtner H-O (1994) Physiologial and metabolic responses to hypoxia in invertebrates. Rev Physiol Biochem Pharmacol 125:43–147

    PubMed  CAS  Google Scholar 

  • Hackstein JH, Tjaden J, Huynen M (2006) Mitochondria, hydrogenosomes and mitosomes: products of evolutionary tinkering! Curr Genet 50:225–245

    PubMed  CAS  Google Scholar 

  • Hackstein JHP, Tjaden J, Koopman W (2007) Hydrogenosomes (and related organelles, either) are not the same. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 135–160

    Google Scholar 

  • Heifetz PB, Förster B, Osmond CB, Giles LJ, Boynton JE (2000) Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol 122:1439–1446

    PubMed  CAS  Google Scholar 

  • Hoffmeister M, van der Klei A, Rotte C, van Grinsven KWA, van Hellemond JJ, Henze K, Tielens AGM, Martin W (2004) Euglena rhodoquinone : ubiquinone ratio and mitochondrial proteome differ under aerobic and anaerobic conditions. J Biol Chem 279:22422–22429

    PubMed  CAS  Google Scholar 

  • Holland HD (1999) When did the Earth's atmosphere become oxic? Geochem News 100:20–22

    Google Scholar 

  • Holland HD, Beukes N (1990) A paleoweathering profile from Griqualand West, South Africa: Evidence for a dramatic rise in atmospheric oxygen between 2.2 and 1.9 BYBP. Am J Sci 290A:1-34

    Google Scholar 

  • Horner DS, Heil B, Happe T, Embley TM (2002) Iron hydrogenases – ancient enzymes in modern eukaryotes. Trends Biochem Sci 27:148–153

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hurtgen MT (2003) Ancient oceans and oxygen. Nature 423:592–593

    PubMed  CAS  Google Scholar 

  • Javaux EJ, Knoll AH, Walter MR (2001) Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412:66–69

    PubMed  CAS  Google Scholar 

  • Jekely G, Arendt D (2006) Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 28:191–198

    PubMed  CAS  Google Scholar 

  • Johnston DT, Wing BA, Farquhar J, Kaufman AJ, Strauss H, Lyons TW, Kah LC, Canfield DE (2005) Active microbial sulfur disproportionation in the Mesoproterozoic. Science 310:1477–1479

    PubMed  CAS  Google Scholar 

  • Kasting JF (1993) Earth's early atmosphere. Science 259:920–926

    PubMed  CAS  Google Scholar 

  • 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) The genome of the intracellular parasite, Encephalithozoon cuniculi. Nature 414:450–453

    PubMed  CAS  Google Scholar 

  • Knoll AH (1992) The early evolution of eukaryotes: A geological perspective. Science 256:622–627

    PubMed  CAS  Google Scholar 

  • Lahti CJ, Bradley PJ, Johnson PJ (1994) Molecular characterization of the alpha-subunit of Trichomonas vaginalis hydrogenosomal succinyl CoA synthetase. Mol Biochem Parasitol 66:309–318

    PubMed  CAS  Google Scholar 

  • Lane N (2007) Mitochondria: Key to complexity. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 13–38

    Google Scholar 

  • Lindmark DG, Müller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate, Tritrichomonas foetus and its role in pyruvate metabolism. J Biol Chem 248:7724–7728

    PubMed  CAS  Google Scholar 

  • Lloyd D, Ralphs JR, Harris JC (2002) Giardia, a eukaryote without hydrogenosomes, produces hydrogen. Microbiology 148:727–733

    PubMed  CAS  Google Scholar 

  • Loftus B, Anderson I, Davies R, Alsmark UC, Samuelson J, Amedeo P, Roncaglia P, Berriman M, Hirt RP, Mann BJ, Nozaki T, Suh B, Pop M, Duchene M, Ackers J, Tannich E, Leippe M, Hofer M, Bruchhaus I, Willhoeft U, Bhattacharya A, Chillingworth T, Churcher C, Hance Z, Harris B, Harris D, Jagels K, Moule S, Mungall K, Ormond D, Squares R, Whitehead S, Quail MA, Rabbinowitsch E, Norbertczak H, Price C, Wang Z, Guillén N, Gilchrist C, Stroup SE, Bhattacharya S, Lohia A, Foster PG, Sicheritz-Ponten T, Weber C, Singh U, Mukherjee C, El-Sayed NM, Petri WA Jr, Clark CG, Embley TM, Barrell B, Fraser CM, Hall N (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433:865–868

    PubMed  CAS  Google Scholar 

  • Mai ZM, Ghosh S, Frisardi M, Rosenthal B, Rogers R, Samuelson J (1999) Hsp60 is targeted to a cryptic mitochondrion-derived organelle (crypton) in the microaerophilic protozoan parasite Entamoeba histolytica. Mol Cell Biol 19:2198–2205

    PubMed  CAS  Google Scholar 

  • Margulis L, Chapman M, Guerrero R, Hall J (2006) The last eukaryotic common ancestor (LECA): Acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon. Proc Natl Acad Sci USA 103:13080–13085

    PubMed  CAS  Google Scholar 

  • Margulis L (1970) Origin of Eukaryotic Cells. Yale University Press, New Haven, p 349

    Google Scholar 

  • Martin W (2007) Eukaryote and mitochondrial origins: Two sides of the same coin and too much ado about oxygen. In: Falkowski P, Knoll AH (eds) Primary Producers of the Sea. Academic Press, New York, pp 55–73

    Google Scholar 

  • Martin W, Dagan T, Koonin EV, Dipippo JL, Gogarten JP, Lake JA (2007) The evolution of eukaryotes. Science 316:542–543

    PubMed  CAS  Google Scholar 

  • Martin W, Koonin EV (2006) Introns and the origin of nucleus-cytosol compartmentalization. Nature 440:41–45

    PubMed  CAS  Google Scholar 

  • Martin W, Rotte C, Hoffmeister M, Theissen U, Gelius-Dietrich G, Ahr S, Henze K (2003) Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 55:193–204

    PubMed  CAS  Google Scholar 

  • Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralbl 25:593–604 [English translation in Eur J Phycol 34:287–295 (1999)]

    Google Scholar 

  • Müller M (2003) Energy metabolism. Part I: Anaerobic protozoa. In: Marr J (ed) Molecular Medical Parasitology. Academic Press, London, pp 125–139

    Google Scholar 

  • Müller M (2007) The road to hydrogenosomes. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 1–12

    Google Scholar 

  • Nicholas WL (1991) Interstitial Meifauna. In: Bryant C (ed) Metazoan Life Without Oxygen. Chapman and Hall, London, pp 129–145

    Google Scholar 

  • Painter HJ, Morrisey JM, Mather MW, Vaidya AB (2007) Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum. Nature 446:88–91

    PubMed  CAS  Google Scholar 

  • Pisani D, Cotton JA, McInerney JO (2007) Supertrees disentangle the chimaeric origin of eukaryote genomes. Mol Biol Evol 24:1752–1760

    PubMed  CAS  Google Scholar 

  • Poulton SW, Fralick PW, Canfield DE (2004) The transition to a sulphidic ocean ∼ 1.84 billion years ago. Nature 431:173–177

    PubMed  CAS  Google Scholar 

  • Preisig O, Zufferey R, Thöny-Meyer L, Appleby CA, Hennecke H (1996) A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178:1532–1538

    PubMed  CAS  Google Scholar 

  • Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MS, Op den Camp HJ, Derksen JW, Pina-Ochoa E, Eriksson SP, Nielsen LP, Revsbech NP, Cedhagen T, van der Zwaan GJ (2006) Evidence for complete denitrification in a benthic foraminifer. Nature 443:93–96

    PubMed  CAS  Google Scholar 

  • 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 fusion of pyruvate:ferredoxin oxidoreductase and NADPH-cytochrome P450 reductase. Mol Biol Evol 18:710–720

    PubMed  CAS  Google Scholar 

  • Runnegar B (1991) Oxygen and the early evolution of the metazoa. In: Bryant C (ed) Metazoan Life Without Oxygen. Chapman and Hall, London, pp 65–87

    Google Scholar 

  • Sack L, Zeyl C, Bell G, Sharbel T, Reboud X, Bernhardt T, Koelewyn H (1994) Isolation of four new strains of Chlamydomonas reinhardtii (chlorophyta) from soil samples. J Phycol 30:770–773

    CAS  Google Scholar 

  • Sagan L (1967) On the origin of mitosing cells. J Theoret Biol 14:225–274

    CAS  Google Scholar 

  • Sanchez LB, Galperin MY, Müller M (2000) Acetyl-CoA Synthetase from the Amitochondriate eukaryote Giardia lamblia belongs to the newly recognized superfamily of acyl-CoA synthetases (nucleoside diphosphate-forming). J Biol Chem 275:5794–5803

    PubMed  CAS  Google Scholar 

  • Sapp J (1994) Evolution by Association: A History of Symbiosis. Oxford University Press, New York, p 255

    Google Scholar 

  • Sapp J (2007) Mitochondria and their host: Morphology to molecular phylogeny. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 57–84

    Google Scholar 

  • Schneider T, Schneider A (1985) Wax ester fermentation in Euglena T. Factors favouring the synthesis of odd-numbered fatty acids and alcohols. Planta 166:67–73

    CAS  Google Scholar 

  • Schöttler U, Bennet EM (1991) Annelids. In: Bryant C (ed) Metazoan Life Without Oxygen. Chapman and Hall, London, pp 165–185

    Google Scholar 

  • Searcy DG (2006) Rapid hydrogen sulfide consumption by Tetrahymena pyriformis and its implications for the origin of mitochondria. Eur J Protistol 42:221–231

    PubMed  Google Scholar 

  • Shen Y, Knoll AH, Walter MR (2003) Evidence for low sulphate and anoxia in a mid-Proterozoic marine basin. Nature 423:632–635

    PubMed  CAS  Google Scholar 

  • Simpson AGB, Inagaki Y, Roger AJ (2006) Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of primitive eukaryotes. Mol Biol Evol 23:615–625

    PubMed  CAS  Google Scholar 

  • Steinbüchel A, Müller M (1986) Anaerobic pyruvate metabolism of Tritrichomonas foetus and Trichomonas vaginalis hydrogenosomes. Mol Biochem Parasitol 20:57–60

    PubMed  Google Scholar 

  • Tachezy J, Dolezal P (2007) Iron–sulfur proteins and iron–sulfur cluster assembly in organisms with hydrogenosomes and mitosomes. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 105–134

    Google Scholar 

  • Theissen U (2006) Die Sulfid:Chinon Oxidoreductase (SQR) des Wattwurms Arenicola marina: Funktion, Mechanismus und Evolution. Dissertation, University of Düsseldorf

    Google Scholar 

  • Tielens AGM, Rotte C, van Hellemond J, Martin W (2002) Mitochondria as we don't know them. Trends Biochem Sci 27:564–572

    PubMed  CAS  Google Scholar 

  • Tielens AGM, van Hellemond JJ (2007) Anaerobic mitochondria: Properties and origins. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 85–104

    Google Scholar 

  • Tovar J, León-Avila G, Sánchez LB, Sutak R, Tachezy J, van der Giezen M, Hernández M, Müller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172–176

    PubMed  CAS  Google Scholar 

  • Tovar J (2007) Mitosomes of parasitic protozoa: Biology and evolutionary significance. In: Martin W, Müller M (eds) Origin of Mitochondria and Hydrogenosomes. Springer, Berlin Heidelberg New York, pp 277–300

    Google Scholar 

  • Tovar J, Fischer A, Clark CG (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba. Mol Microbiol 32:1013–1021

    PubMed  CAS  Google Scholar 

  • Tucci S, Proksch P, Martin W (2007) Fatty acid biosynthesis in mitochondria of Euglena. In: Benning C, Ohlrogge J (eds) Current Advances in the Biochemistry and Cell Biology of Plant Lipids. Pp. Aardvark Global Publishing Company, LLC. Salt Lake City, UT, pp 133–136

    Google Scholar 

  • van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6:525–530

    PubMed  Google Scholar 

  • van der Giezen M, Tovar J, Clark CG (2005) Mitochondrion-derived organelles in protists and fungi. Int Rev Cytol 244:175–225

    PubMed  Google Scholar 

  • van Grinsven KWA, Rosnowsky S, van Weelden SWH, Pütz S, van der Giezen M, Martin W, van Hellemond JJ, Tielens AGM, Henze K (2007) Acetate:succinate CoA-transferase in the hydrogenosomes of Trichomonas vaginalis: identification and characterization. J Biol Chem (in press) [doi:10.1074/jbc.M702528200

    Google Scholar 

  • van Hellemond JJ, van der Klei A, van Weelden SW, Tielens AGM (2003) Biochemical and evolutionary aspects of anaerobically functioning mitochondria. Philos Trans R Soc Lond B 358:205–213

    Google Scholar 

  • van Valen LM, Maiorana VC (1980) The archaebacteria and eukaryotic origins. Nature 287:248–250

    PubMed  Google Scholar 

  • Vetter RD, Powell MA, Somero GN (1991) Metazoan adaptations to sulfide. In: Bryant C (ed) Metazoan Life Without Oxygen. Chapman and Hall, London, pp 109–128

    Google Scholar 

  • Williams BA, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–869

    PubMed  CAS  Google Scholar 

  • Wolfe AJ (2005) The acetate switch. Microbiol Mol Biol Rev 69:12–50

    PubMed  CAS  Google Scholar 

  • Yarlett N (1994) Fermentation product formation. In: Mountfort DO, Orpin CG (eds) Anaerobic Fungi: Biology, Ecology and Function. Marcel Dekker, New York, pp 129–146

    Google Scholar 

  • Yarlett N, Orpin CG, Munn EA, Yarlett NC, Greenwood CA (1986) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236:729–739

    PubMed  CAS  Google Scholar 

  • Yong R, Searcy DG (2001) Sulfide oxidation coupled to ATP synthesis in chicken liver mitochondria. Comp Biochem Physiol B 129:129–137

    PubMed  CAS  Google Scholar 

  • Zebe E (1991) Arthropods. In: Bryant C (ed) Metazoan Life Without Oxygen. Chapman and Hall, London, pp 218–237

    Google Scholar 

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  1. Institute of Botany, University of Düsseldorf, Universitätsstr. 1, 40225, Düsseldorf, Germany

    William Martin

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Jan Tachezy

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Martin, W. (2007). Anaerobic Eukaryotes in Pursuit of Phylogenetic Normality: the Evolution of Hydrogenosomes and Mitosomes. In: Tachezy, J. (eds) Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Microbiology Monographs, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2007_108

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