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Mitochondria and Hydrogenosomes Are Two Forms of the Same

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Mitochondria and Hydrogenosomes Are Two Forms of the Same Publishedonline 12December 2002 Mitochondriaandhydrogeno somesare twoforms of the samefundamenta lorganelle T.Martin Embley * ,Mark van der Giezen † ,David S.Horner ‡ , Patricia L.Dyaland Peter Foster Departmentof Zoology, The Natural History Museum, CromwellRoad, London SW75BD, UK Publisheddata suggestthat hydrogenosomes,organelles foundin diverseanaerobic eukaryotesthat make energy andhydrogen, were once mitochondria. Ashydrogenosomes generally lack agenome,the conver- sionis probably oneway. The sourcesof thekey hydrogenosomal enzymes,pyruvate :ferredoxin oxido- reductase(PFO) andhydrogenase, are notresolved by currentphylogenetic analyses,but it is likely that both werepresent at an early stage ofeukaryotic evolution.Once thought toberestricted to a fewunusual anaerobic eukaryotes,the proteins are intimately integrated intothe fabric ofdiverse eukaryotic cells, wherethey are targeted todifferent cell compartments,and not just hydrogenosomes. There isno evidence supporting theview that PFO andhydrogenase originated from themitochondrial endosymbiont,as pos- itedby thehydrogen hypothesisfor eukaryogenesis.Other organelles derivedfrom mitochondria have nowbeen described in anaerobic andparasitic microbial eukaryotes,including speciesthat wereonce thought tohave diverged beforethe mitochondrial symbiosis.It thusseems possible that all eukaryotes may eventually beshown to contain an organelle ofmitochondrial ancestry,to which differenttypes of biochemistry canbe targeted. It remains tobe seen if, despite their obviousdifferences, this family of organelles sharesa commonfunction of importance for theeukaryotic cell,other than energy production, that might provide theunderlying selectionpressure for organelle retention. Keywords: hydrogenosomes;mitochondria; eukaryotic evolution;hydrogenase 1. INTRODUCTION 2. ORIGINOF THE ORGANELLECOMPARTMENT Hydrogenosomesare anaerobic organelles that make Shortly after hydrogenosomeswere discovered in Tri- energy andexcrete molecular hydrogen,aiding redox bal- trichomonasfoetus by Lindmark &Mu¨ller (1973) it was ancing,which are foundin phylogenetically diverseeukar- suggestedthat thesehydrogenosomes were descended yotes (Mu¨ller 1993; Biagini et al. 1997a).The beststudied from endosymbioticclostridia, aeubacterial group that hydrogenosome-containinggroups are trichomonads,cili- also makeshydrogen usinghydrogenase and PFO, provid- atesand chytrid fungi butother eukaryotesliving in anaer- ing acommonorigin for organelles andbiochemistry obic habitats probably also containthem (seeBroers et al. (Whatley et al. 1979). The subsequentdemonstration of a 1993; Fenchel& Finlay 1995; Roger &Silberman 2002). doublemembrane aroundthe hydrogenosomes of T. foetus Hydrogenosomeshave thusbeen frequently invented (Benchimol &DeSouza1983), wasseen as being consist- independentlyduring eukaryotic evolution,and the ques- entwith anendosymbiotic origin. Atthat time, Tricho- tionof how we currently think eukaryoteshave achieved monas andrelated trichomonadssuch as Tritrichomonas this is thefocus of this shortreview. Two key issuesmust that composethe Parabasalia, werethought neverto have beaddressed: had any mitochondria. Parabasalids wereone of four protozoan groups placedby Cavalier-Smith (1983) into (i) thesource(s) of the organelle compartment housing theeukaryotic subkingdomArchezoa, the others being thehydrogen-producing biochemistry; and Archamoebae (e.g. Entamoeba),Metamonada(e.g. (ii) thesource(s) of the biochemistry itself,in particular Giardia, Spironucleus )andMicrospora (e.g. Vairimorpha , thekey enzymes(Mu ¨ller 1993), PFO andhydro- Trachipleistophora ).Archezoa weredefined as being primi- genase. tively withoutmitochondria becausethey split from other eukaryotesbefore the mitochondrial symbiosis (Cavalier- Smith 1983). The first molecular data tosuggest that Trichomonas *Authorfor correspondence ([email protected]). vaginalis (andby inferenceits relatives) oncecontained the † Present address: Schoolof BiologicalSciences, RoyalHolloway, Univer- mitochondrionendosymbiont, were discoveries of genes sityof London, Egham, Surrey TW20 0EX,UK. ‡ Present address: Dipartimentodi Fisiologia e BiochimicaGenerali, Uni- encodingmitochondrial-type heat shockproteins (Hsp70, versity of Milan,via Celoria 26,20133 Milan, Italy. Hsp60 andHsp10), on its nucleargenome (Bui et al. One contribution of 21to a DiscussionMeeting Issue ‘Chloroplastsand 1996; Germot et al. 1996; Horner et al. 1996; Roger et al. mitochondria: functional genomics and evolution’. 1996). In aerobic organisms, theseproteins have key roles Phil. Trans. R.Soc. Lond. B (2003) 358, 191–203 191 Ó 2002 TheRoyal Society DOI 10.1098/rstb.2002.1190 192T. M.Embley andothers Evolution of hydrogenosomes in mitochondria, andphylogenetic analysis betrays their sequencesand some of these have also beenshown to be commonorigin from theendosymbiont that gave rise to cleavedduring transit (Plumper et al. 1998). For example, theorganelle (Boorstein et al. 1994; Viale &Arakaki in vitro import experiments onhydrogenosomal ferredoxin 1994). The Trichomonas Hsp60 formeda monophyletic showthat it carries acleavable eight amino-acid N-ter- group with mitochondrial Hsp60,which wasmost closely minal extension,that is necessaryfor import into isolated related tothe homologous protein GroELfrom a-proteo- Trichomonas hydrogenosomes(Bradley et al. 1997). The bacteria. This is thebacterial group from which themito- sametargeting sequencecan also sorta marker protein chondrial endosymbiontis thought tohave originated into yeastmitochondria (Ha¨usler et al. 1997). Amember (Viale &Arakaki 1994; Andersson et al. 1998; Gray et al. ofthe mitochondrial carrier family ofproteinshas recently 1999). The simplest interpretation ofthesedata is that the beenisolated from Trichomonas hydrogenosomes(Dyall et gene for Trichomonas Hsp60 also came from themito- al. 2000). Theseproteins are foundin theinner mem- chondrial endosymbiont.The GroELfrom clostridia clus- brane ofmitochondria andare imported usingcryptic teredin aseparate part ofthe tree, well away from the internal signals (Pfanner& Geissler2001). The Tricho- Trichomonas andmitochondrial proteins(Horner et al. monas protein,which is ofunknown function, can also be 1996). The localization ofthe Hsp60 in Trichomonas imported into yeastmitochondria, strongly suggesting that hydrogenosomes(Bui et al. 1996; Bozner1997), provided thesesignals are conserved.In thereciprocal experiment, thefirst strong data that theorganelle itself sharedcom- Trichomonas hydrogenosomescan import theyeast AAC monancestry with mitochondria. Trichomonas hydro- protein,confirming that theimport machinery required to genosomes,like mitochondria, divide by segmentationand recognizethe yeast-import signals is also presentin the partition (Benchimol et al. 1996). hydrogenosome(Dyall et al. 2000). The hypothesisthat Trichomonas Hsp60 andHsp70 At least fourphylogenetically distinctgroups ofanaer- originated from thesame symbiont that gave rise tomito- obic ciliates containhydrogenosomes (see Embley et al. chondria is thesimplest interpretation ofthese data. By 1995), suggesting that thetransition from aerobe with contrast,alternative theorieshave positedhorizontal gene mitochondria toanaerobe with hydrogenosomes,is fairly transferfrom another a-proteobacterium (Sogin 1997), easyto make within this group ofpredominantly aerobic from foodbacteria (Doolittle 1998) or from ‘more casual eukaryotes.Hydrogenosomal ciliates are ecologically sig- donors’ (Kurland& Andersson2000), toexplain thepres- nificant,providing anichefor endosymbioticmethanog- enceof Hsp genes on the genomes of Trichomonas and ensthat usethe hydrogen andcarbon dioxide liberated by other Archezoa.However, none of these alternatives are thehydrogenosomes, to make methaneand energy foundedin phylogenetic analysesthat actually indicatean (Fenchel1993; Embley &Finlay 1994). It has been alternative donorto the mitochondrial endosymbiont. argued that thefacility by which ciliates make hydro- RecentHsp60 treescontaining Trichomonas and Giardia genosomesmust result from modification ofpre-existing are consistentwith currentideas of their relationships mitochondria (Embley et al. 1995), andin somespecies, (Embley &Hirt 1998; Roger 1999), andthus with vertical for example Metopuscontortus and Cyclidium porcatum , the inheritance ofgenes from ancestorsthat containedthe hydrogenosomesstrongly resemblemitochondria in their mitochondrial endosymbiont(see Horner & Embley morphology (Finlay &Fenchel1989; Fenchel& Finlay 2001). There are nowadditional data that strongly sup- 1995). The hydrogenosomesof M.contortus also resemble port alink between Trichomonas hydrogenosomesand mitochondria physiologically, being calcium storesand mitochondria. possessinga membrane potential andan alkali lumen Trichomonas hydrogenosomeslack an associatedgen- (Biagini et al. 1997b).At least oneciliate, Nyctotherus ome(Clemens & Johnson2000), sotheir proteinsmust ovalis,apparently containsa mitochondrial small subunit besynthesized in thecytosol and then correctly targeted ribosomal RNA gene(Akhmanova et al. 1998). Although andimported. In mitochondria thereare twomain protein thegene product has notbeen localized tothe ciliate import pathways, eachof which is basedupon a sophisti- hydrogenosome,such genes are normally encodedby the catedmulticomponent pathway that sharessome common mitochondrial genome(Gray et al. 1998). Thus,in at least proteins(Pfanner & Geissler2001). The mitochondrial onecase, there is thepossibility that aciliate hydrogeno-
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