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May 2000 Comment

May 2000 Comment

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stage for the genesis of the first and date there are no ‘ancient’ protists (or Comment provides a much attention has therefore centred on these Archezoa) which have been shown to be platform for readers of Microbiology to ‘anaerobic’ . The milestone in this strictly anaerobic. communicate their personal observations evolution is the endosymbiosis of the mito- Strict anaerobes can however be found in and opinions in a more informal way than chondria and thus the passage from an anaer- the crown of the eukaryotic tree. Ciliates, such through the submission of papers. obic to an aerobic way of . Here, we would as Metopus contortus and Parablepharisma Most of us feel, from time to time, that like to briefly illustrate how this notion of a sp., do not survive for more than a few hours other authors have not acknowledged the link between anaerobiosis and primitism is when exposed to aerobic conditions and work of our own or other groups or have unfounded and how it has misled subsequent require strict omission of O2 for growth omitted to interpret important aspects hypotheses for the evolution of the eukaryotic (15). However, even in these , the of their own data. Perhaps we have cell. capacity for anaerobic biosynthetic metabo- observations that, although not sufficient To discuss anaerobicity it is paramount to lism has not been demonstrated. Phylogenetic to merit a full paper, add a further be clear as to its definition. To describe an studies of these organisms clearly show that dimension to one published by others. as anaerobic because O2 is not they have derived, on several occasions, from In other instances we may have a useful required for oxidative phosphorylation is aerobic ciliates (12). Interestingly, examples of piece of methodology that we would practical in many circumstances, but may be microaerobic ciliates behaving as facultative like to share. misleading in this context. Biochemically, a anaerobes have been described in the labora- true anaerobic organism should be able to tory (2). Strict anaerobic ciliates also contain The Editors hope that readers will take carry out all its metabolic functions, such and in some cases, such as full advantage of this section and use it as sterol and fatty acid metabolism, anaero- in Cyclidium and Cristigera, both mitochon- to raise matters that hitherto have been bically, without the need to scavenge meta- dria- and -bearing species are confined to a limited audience. bolic constituents from its environment. A found within the same ciliate genus (16, 14). Jon Saunders, Editor-in-Chief distinction must also be made as to whether an organism is aerotolerant or whether it Problems with current benefits from low levels of O2. mitochondrial hypotheses Primitive anaerobic The first misconception regarding anaero- protozoa: a false concept? Primitive ‘anaerobic’ protozoa bicity and eukaryotic antiquity arose from the somewhat artificial establishment of enjoy just a little O2 Since Bütschli (7), protistologists have tried ‘Anaerobic’ protozoa lack electron-linked the amitochondriate protozoan group, the to not only organize the interrelationships oxidative phosphorylation. They do, how- Archezoa (9). By various phylogenetic means [but mainly by nuclear small subunit (SSU) between the different groups of protists, but ever, take up O2 at high rates and some also to build phylogenetic trees to explain the have been observed to have higher affinities rRNA analysis], the Archezoa were inferred

evolution of the eukaryotic cell. In the last 20 for O2 than their aerobic counterparts years, results obtained by molecular tech- containing cytochrome oxidase (4, 21). Low ᭤ GUIDELINES niques and electron microscopy have furnished levels of O have been shown to affect the 2 Communications should be in the form general ideas on what the tree of life may look carbon balance of and Hexamita (26, of letters and should be brief and to the like. The base of the tree generally includes 5), both belonging to the diplomonads, until point. A single small Table or Figure may groups such as Metamonada (e.g. Giardia, recently generally favoured as forming the be included, as may a limited number of Hexamita and Trepomonas), Microsporidia deepest branching eukaryotic group (20). references (cited in the text by numbers, and Parabasala (e.g. vaginalis, , far from being anaer- and listed in alphabetical order at the end Pseudotrichomonas keilini) (9). obic, requires traces of O for optimal growth 2 of the letter). A short title (fewer than 50 These basal ‘anaerobic’ protozoa differ and reproduction (25). Why O is required by 2 characters) should be provided. from aerobic cells by the absence of mitochon- these organisms is not known for certain, but dria and hence oxidative phosphorylation. part of the reason may be to recycle electron Approval for publication rests with Energy generation is derived from glycolysis acceptors such as NAD(P)+ (unpublished the Editor-in-Chief, who reserves the with some unusual features (i.e. some enzymes observations from our laboratories in fact right to edit letters and/or to make a

are pyrophosphate-dependent) and also from conclude that in growth conditions where O2 brief reply. Other interested persons may alternative substrate (i.e. the has been strictly omitted, some diplomonads also be invited to reply. The Editors arginine dihydrolase pathway). Some of them fail to grow). Therefore, the correct term to of Microbiology do not necessarily (e.g. the trichomonads) also possess unusual describe these organisms should be micro- agree with the views expressed in redox organelles known as hydrogenosomes aerophilic. A strict anaerobe in this context Microbiology Comment.

which, as well as other products, generate H2 will be defined as an organism which is (giving them their name). highly susceptible to O and which will grow Contributions should be addressed to the 2 Editor-in-Chief via the Editorial Office. Early anoxic has been set as the optimally in an O2-free environment. To

Microbiology 146, May 2000 1019 Microbiology Comment

as being primitive and anaerobic, urging explain the absence of DNA in hydrogeno- free-living diplomonad Hexamita sp. J Euk Microbiol 44, the notion that the organism which first somes. However, it has been shown recently 447–453. 5. Biagini, G. A., McIntyre, P. S., Finlay, B. J. & Lloyd, D. harboured the mitochondrial endosymbiont that the hydrogenosome-bearing symbiotic (1998). Carbohydrate and amino acid fermentation in the was a primitive anaerobic protozoan. This ciliate Nyctotherus contains DNA (as con- free-living primitive protozoon Hexamita sp. Appl hypothesis, however, has now generally been firmed by immunocytochemistry) (1). Further- Environ Microbiol 64, 203–207. rejected. Over the past few years, genes of more, this recent study revealed that rDNA 6. Budin, K. & Philippe, H. (1998). New insights into the mitochondrial origin have been shown to phylogeny of based on ciliate Hps 70 from Nyctotherus hydrogenosomes shows high sequences. Mol Biol Evol 15, 943–956. be present in these Archezoa (namely the sequence similarity to mitochondrial SSU 7. Bütschli, O. (1880–1889). Protozoa I, II, III. In Klassen microsporidia, Giardia and Trichomonas; see rRNA genes from aerobic ciliates: surely, the und Ordnung des Their-reichs. Leipzig. recent review, 11). Furthermore, there are nail in the coffin for the die-hard sceptic of a 8. Cavalier-Smith, T. (1987). The simultaneous symbiotic growing concerns as to the use of single mitochondrial origin for hydrogenosomes. origin of mitochondria, chloroplasts and microbodies. Ann N Y Acad Sci 503, 55–72. genes to confer phylogenetic relationships. Taking into account the probable mono- 9. Cavalier-Smith, T. (1993). Kingdom protozoa and its Significantly, recent studies now favour the phyletic origin of mitochondria, there is 18 phyla. Microbiol Rev 57, 953–994. ‘Archezoan’ microsporidia species to be more increasing evidence to suggest that the origin 10. Edlin, T. D., Li, J., Visvesvara, G. S., Vodkin, M. H., closely related to fungi than protists (e.g. 10, of the eukaryotic cell and its mitochondrial McLaughlin, G. L. & Katiyar, S. K. (1996). Phylogenetic analysis of beta-tubilin sequences from amitochondrial 19). It has been suggested that the primitive component came into being simultaneously protozoa. Mol Phylogenet Evol 5, 359–367. status enjoyed by the diplomonads is also rather than sequentially as the serial endosym- 11. Embley, T. M. & Hirt, R. P. (1998). Early branching proving increasingly tenuous (e.g. 6). biosis hypothesis would predict (18). There is eukaryotes? Curr Opin Genet Dev 8, 624–629. The demonstration of an anaerobic origin no compelling evidence, however, that this 12. Embley, T. M., Finlay, B. J., Dyal, P. L., Hirt, R. P., for eukaryotes was again perpetuated in Wilkinson, M. & Williams, A. G. (1995). Multiple origins phenomenon occurred in the absence of O2 or of anaerobic ciliates with hydrogenosomes within the the recent ‘ hypothesis’ (23). This that the symbiont which gave rise to the mito- radiation of aerobic ciliates. Proc R Soc Lond B 262, 87–93. hypothesis argues that the original eukaryote chondrion was anaerobic. It is our interpre- 13. Embley, T. M., Horner, D. S. & Hirt, R. P. (1997). was derived from an association between a tation of the available evidence that (i) the Anaerobic eukaryotic evolution: hydrogenosomes as H -producing proteobacterium and an auto- primitive status of Archezoa is precarious, (ii) biochemically modified mitochondria? Trends Ecol Evol 2 12, 437–441. trophic archaeon, describing how in some ‘ancient’ anaerobic protozoa described to 14. Esteban, G., Guhl, B. E., Clarke, K. J., Embley, T. M. circumstances this association gave rise to date are not true anaerobes, but more likely & Finlay, B. J. (1993). Cyclidium porcatum n. sp.: a free- hydrogenosomes whilst in others it gave rise have adapted to an anaerobic lifestyle (para- living anaerobic scuticociliate containing a stable to mitochondria. This prediction, however, is sitic or free-living) and probably at some stage complex of hydrogenosomes, eubacteria and archaebacteria. Eur J Protistol 32, 293–297. contrary to the simplest explanation that contained mitochondria, and (iii) there is 15. Fenchel, T. & Finlay, B. J. (1990). toxicity, hydrogenosomes are an adaptation of pre- more substantial evidence to suggest that respiration and behavioural responses to oxygen in free- existing mitochondria (3, 13). hydrogenosomes are a secondary modifica- living anaerobic ciliates. J Gen Microbiol 136, 1953–1959. The hydrogenosome until recently tion of mitochondria, therefore refuting (at 16. Fenchel, T. & Finlay, B. J. (1991). The biology of free- enjoyed an enigmatic reputation. Since its living anaerobic ciliates. Eur J Protistol 26, 201–215. least in part) the recent ‘hydrogen’ and 17. Finlay, B. J. & Fenchel, T. (1989). Hydrogenosomes in discovery some 25 years ago, the origin of ‘’ hypotheses (23, 22). some anaerobic protozoa resemble mitochondria. FEMS this organelle has been under debate. A vision of prebiotic Earth as a mass of Microbiol Lett 65, 311–314. Characterization of key enzymes such as bubbling rock and toxic fumes is perhaps too 18. Gray, M. W., Burger, G. & Franz-Lang, B. (1999). pyruvate : ferredoxin oxidoreductase led tantalizing for evolutionists to ignore when Mitochondrial evolution. Science 283, 1476–1481. 19. Hirt, R. P., Longsdon, J. M., Healy, B., Dorey, M. W., early workers to hypothesize that hydrogeno- dealing with the origin of eukaryotic life. Doolittle, W. F. & Embley, T. M. (1999). Microsporidia somes derived from an endosymbiosis with However, closer examination of aerobic as are related to fungi: evidence from the largest subunit of Clostridia-like (24). Unlike proto- well as anaerobic protozoa may, in our RNA polymerase II and other proteins. Proc Natl Acad zoan hydrogenosomes which are bound by opinion, be just as fruitful. Sci USA 96, 580–585. 20. van Keulen, H., Guttell, R. R., Gates, M. A., two membranes, fungal hydrogenosomes Campbell, S. R., Erlandsen, S. L., Jarroll, E. L., Kulda, J. (e.g. chytrid fungi) appeared to possess only 1 & Meyer, E. A. (1993). Unique phylogenetic position of Giancarlo A. Biagini * and diplomonadida based on the complete small subunit one membrane and were argued to have 2 derived from peroxisomes (8). Finally, free- Catherine Bernard ribosomal RNA sequence of Giardia ardeae, G. muris, G. living ciliate hydrogenosomes which possess duodenalis and Hexamita spp. FASEB J 7, 223–231. 1 21. Lloyd, D., Williams, J., Yarlett, N. & Williams, A. G. characteristic mitochondria-like folding of School of Biochemistry & Molecular (1982). Oxygen affinities of the hydrogenosome- the inner membrane, prompted the notion of Biology, University of New South Wales, containing protozoa Tritrichomonas foetus and a mitochondrial origin (17). In the last few Sydney 2052, Australia Dasytricha ruminantium, and two aerobic protozoa, 2School of Science, University of Western determined by bacterial bioluminescence. J Gen years, there has been overwhelming evidence Microbiol 128, 1019–1022. (reviewed in 3 and 13) in molecular (e.g. Sydney Nepean, Kingswood 2747, Australia 22. López-García, P. & Moreira, D. (1999). Metabolic presence of mitochondrial chaperonin genes *For correspondence. symbiosis at the origin of eukaryotes. Trends Biochem Sci 24, 88–93. in hydrogenosome-bearing protozoa), physi- Tel: +61 2 9385 2043. Fax: +61 2 9385 1483. ological (e.g. hydrogenosomes possess a 23. Martin, W. & Müller, M. (1998). The hydrogen e-mail: [email protected] hypothesis for the first eukaryote. Nature 392, membrane potential and act as calcium 37–41. stores) and morphological (e.g. the reasser- 1. Akhmanova, A., Voncken, F., van Alen, T., van Hoek, 24. Müller, M. (1980). The hydrogenosome. In The tion that fungal hydrogenosomes possess two A., Boxma, B., Vogels, G., Veenhuis, M. & Hackstein, Eukaryotic Microbial Cell, 30th Symposium of the membranes) studies to strongly support a J. H. (1998). A hydrogenosome with a genome. Nature Society for General Microbiology, pp. 127–142. Edited by 396, 527–528. G. W. Gooday, D. Lloyd & A. P. J. Trinci. Cambridge: mitochondrial origin for hydrogenosomes. 2. Bernard, C. & Fenchel, T. (1996). Some Cambridge University Press. The lack of a detectable hydrogenosomal microaerophilic ciliates are facultative anaerobes. Eur J 25. Paget, T. A. & Lloyd, D. (1990). Trichomonas genome and therefore the lack of an Protistol 32, 293–297. vaginalis requires traces of oxygen and high evolutionary molecular fingerprint has 3. Biagini, G. A., Finlay, B. J. & Lloyd, D. (1997). concentrations of for optimal growth. Evolution of the hydrogenosome. FEMS Microbiol Lett Mol Biochem Parasitol 41, 65–72. been responsible for the speculation about 155, 133–140. 26. Paget, T. A., Kelly, M., Jarrol, E. L., Lindmark, D. G. ancestry. The loss of respiratory function 4. Biagini, G. A., Suller, M. T., Finlay, B. J. & Lloyd, D. & Lloyd, D. (1993). Effects of oxygen on fermentation in (i.e. lack of detectable cytochromes) would (1997). Oxygen uptake and responses of the Giardia lamblia. Mol Biochem Parasitol 57, 65–72.

1020 Microbiology 146, May 2000 Primitive anaerobic tions from the ancestors of organelles, also in that today contains , the only protozoa: the wrong host amitochondriate protists (5, 8, 20, 21). currently known to contain Eukaryotes thus seem to have acquired the histones (26). for mitochondria and heterotrophic lifestyle that they now use, Is the view that hydrogenosomes are a hydrogenosomes? raising the question of how they synthesized ‘secondary modification’ of mitochondria at their ATP prior to that acquisition. Third, odds with the hydrogen hypothesis? No, Since Mereschkowsky (22), thoughts on the formulations of the endosymbiont hypothesis because this is just a roundabout way of nature of the most primitive kinds of cells that that focus on the role of oxygen in the origin saying that hydrogenosomes and mitochon- we now call eukaryotes have entailed the of mitochondria (e.g. 2) cannot directly dria share a common ancestor, since, obvi- notion that some cytoplasmic organelles account for data indicating a common ously, no contemporary hydrogenosomes can arose from free-living bacteria through ancestry of mitochondria and hydrogeno- have arisen through modification of contem- endosymbiosis. Endosymbiotic hypotheses somes – the double-membrane-bound, ATP- porary mitochondria. Rather, they must have have fared extremely well when it comes producing organelles of many protists that arisen from mitochondria that existed in the to pinpointing the similarities between shun oxygen-containing (23, 24). past. So what were those ancient mitochon- organelles and free-living bacteria as evidence Indeed, hydrogenosomes (and ATP synthesis dria like in terms of biochemical properties? in favour of their endosymbiotic origin, both in anaerobic mitochondria in general) have Were they like the mitochondria of the in the case of chloroplasts (22) and mito- been a thorn in the side of the endosymbiont Fusarium that perform nitrate and nitrite chondria (30). But for organelles to take up hypothesis, having been difficult to incorpo- respiration, just as many facultatively anaer- residence in a cytoplasm, there had to be a rate into traditional views (16, 23, 27) or obic bacteria do (16)? Were they like host. Endosymbiotic hypotheses for the having been disregarded (19). Given these plathelminth mitochondria that perform origin of mitochondria have had much more newer findings, it is not unreasonable to fumarate respiration as many facultatively success explaining the origins of the organelle question the view that the host may have been anaerobic bacteria do (27)? Were they like the than they have had with explaining the origin a hypothetical, heterotrophic, primitively mitochondria of the ciliate Nyctotherus that of the host. So what was the host? amitochondriate eukaryote, and to pursue produce H2 with the help of a hydrogenase Anaerobic protists play an important role alternative avenues of thought. like hydrogenosomes do (1)? Were they like in this issue because the host for the origin of The hydrogen hypothesis (20) is such an kinetoplastid mitochondria, which use mitochondria has traditionally been envis- alternative, one that specifically addresses the acetate:succinate CoA transferase to regen- aged, either explicitly or implicitly, as a compartmentalization and the ancestral state erate CoASH like hydrogenosomes do (29)? heterotrophic cell with a glycolytic pathway of eukaryotic ATP synthesis. It avoids Or were they like the mitochondria of that did not depend on molecular oxygen for the need to assume that primitively amito- Euglena that, instead of the pyruvate ATP synthesis, like contemporary protists chondriate protists ever existed, because it dehydrogenase complex, use ferredoxin- that have such a lifestyle. In some versions of entails the premise that the host was an dependent pyruvate:NADP oxidoreductase the endosymbiont hypothesis, the host is Archaebacterium, not a eukaryote. It avoids in a reaction that is very similar to that of envisaged as a , but in most versions the need to assume that the host was a pyruvate:ferredoxin oxidoreductase (PFO) in it is envisaged as a eukaryote that either arose because it posits that the host was hydrogenosomes (14)? autogenously (without symbiosis) or as the an autotroph, one that was strictly dependent These questions are intended to make the result of a symbiosis of cells that occurred upon molecular hydrogen as an energy and point that there are a number of anaerobic (but prior to the origin of mitochondria (for a electron source. Through explicitly formu- not necessarily strictly anaerobic) mitochon- random sample see 3, 6, 9, 11, 12, 15, 18, 19, lated selective pressures for gene transfer from dria known that possess and use enzymes 22). But in all versions of the ‘classical’ symbiont to host chromosomes, it directly and/or pathways that are common to faculta- endosymbiont hypothesis that make a state- accounts for the finding that eukaryotes tively anaerobic bacteria and/or hydrogeno- ment on the issue (e.g. 3, 9, 15), the host that studied to date tend to possess a eubacterial somes. As the simplest alternatives to explain acquired the is envisaged as a rather than an archaebacterial glycolytic this observation, either (a) mitochondria arose heterotroph, one that satisfied its ATP needs pathway. It also directly accounts for findings from strictly aerobic bacteria that did not with the help of the glycolytic pathway. that indicate a common ancestry of mito- possess genes for enzymes of anaerobic ATP- At present, the endosymbiont hypothesis chondria and hydrogenosomes, because it producing pathways as found in hydrogeno- has three problems. First, it no longer has a posits that the symbiont was a facultatively somes, in which case the enzymes germane to host. This is because available data indicate anaerobic α-proteobacterium, one that was hydrogenosomal metabolism in the various that contemporary amitochondriate protists able to synthesize ATP either through oxygen- eukaryotic lineages that possess hydrogeno- investigated thus far – organisms which were consuming electron transport like mitochon- somes can be predicted to have been acquired thought to be descendants of the host – dria or through hydrogen-producing fermen- through independent lateral gene transfers, or possessed a mitochondrion in their evolu- tations like hydrogenosomes, dependent upon (b) the genetic starting material for this tionary past, but subsequently lost the environmental conditions. The hydrogen biochemical diversity was present in a faculta- organelle through reduction (summarized in hypothesis thus differs from previous views tively anaerobic bacterium that was the 9, 10, 12, 20, 25). These findings indicate that both on the origins of mitochondria and on the common ancestor of mitochondria and such cells can therefore hardly be descendants nature of the host. It generates some of the hydrogenosomes (20). Under the first alterna- of the host in the endosymbiont hypothesis same predictions as the endosymbiont hypoth- tive, the homologous enzymes in hydrogeno- and they furthermore intertwine the issues of esis does, for example that the respiratory somes of different eukaryotic lineages should the origin of mitochondria and the origin of pathways of oxygen-consuming mitochondria be shown to stem from independent lateral eukaryotes even more tightly than before (9, and α- should be homologous, transfers involving different prokaryotic 10, 12). Second, there is no clear evidence to but it generates different predictions about donors. Under the second alternative, the suggest that the host was even a heterotroph. the origins of pathways of ATP synthesis homologous enzymes in hydrogenosomes of This is because nuclear genes for enzymes of in hydrogenosomes than the endosymbiont different eukaryotic lineages should be shown the glycolytic pathway in the eukaryotic hypothesis does. It furthermore generates to stem from a single eubacterial source (13). cytosol – the backbone of heterotrophy in very different predictions about the host, for More molecular data from eukaryotes that eukaryotes and the pathway that feeds mito- example that the host ultimately should possess hydrogenosomes and ‘atypical’ mito- chondria – appear themselves to be acquisi- descend from the lineage of Archaebacteria chondria are needed.

Microbiology 146, May 2000 1021 Microbiology Comment

None of this is to detract from the impor- of a hydrogenosomal genome bears out one of 12. Gray, M. W., Burger, G. & Lang, B. F. (1999). tance of the observation that many eukary- the predictions of the hydrogen hypothesis, Mitochondrial evolution. Science 283, 1476–1481. 13. Horner, D. S., Hirt, R. P. & Embley, T. M. (1999). otes commonly designated as ‘anaerobic’ rather than refuting it (in part or otherwise). A single eubacterial origin of eukaryotic do grow more prolifically when a bit of A vision of the host as a primitive eukaryote pyruvate:ferredoxin oxidoreductase genes: implications oxygen is present and can be designated as that never possessed mitochondria is perhaps for the evolution of anaerobic eukaryotes. Mol Biol Evol microaerophilic. In the example of the kine- too tantalizing for evolutionists to ignore when 16, 1280–1291. 14. Hrdy, I. & Müller, M. (1995). Primary structure and toplastids, this appears to have to do with the dealing with the origin of this ATP-producing eubacterial relationship of the pyruvate:ferredoxin maintenance of redox balance, i.e. the regen- organelle in its various aerobic and anaerobic oxidoreductase of the amitochondriate eukaryote eration of NAD+ (7). When oxygen is present, manifestations (20, 23–25, 27). The hydrogen Trichomonas vaginalis. J Mol Evol 41, 388–396. bloodstream forms of trypanosomes can hypothesis predicts that upon closer examina- 15. John, P. & Whatley, F. R. (1975). Paracoccus + denitrificans and the evolutionary origin of the regenerate additional NAD from glycolytic tion of aerobic as well as anaerobic protozoa, mitochondrion. Nature 254, 495–498. NADH with the help of a glycerol-3-phos- none will be found that are primitively amito- 16. Kobayashi, M., Matsuo, Y., Takimoto, A., Suzuki, S., phate oxidase, such that one mole of water chondriate. Indeed, if eukaryotes are ever Maruo, F. & Shoun, H. (1996). Denitrification, a novel and two moles pyruvate per mole of found that can be conclusively shown to have type of respiratory metabolism in fungal mitochondrion. J Biol Chem 271, 16263–16267. are produced as waste products. When no never possessed a mitochondrial symbiont in 17. Linstead, D. J. & Bradley, S. (1988). The purification oxygen is available, one mole each of glycerol their evolutionary history, the hydrogen and properties of two soluble reduced and pyruvate are excreted as end products hypothesis would be falsified. The endosym- nicotinamide:acceptor oxidoreductases from to maintain redox balance (7). In other biont hypothesis is currently in search of a Trichomonas vaginalis. Mol Biochem Parasitol 27, 125–133. ‘anaerobic’ or ‘microaerophilic’ protists such formulation that is sufficiently explicit as to 18. Lopez-Garcia, P. & Moreira, D. (1999). Metabolic as trichomonads and diplomonads, which generate similarly falsifiable predictions about symbiosis at the origin of eukaryotes. Trends Biochem generate ATP solely through extended glycol- the host that acquired mitochondria. That Sci 24, 88–93. ysis (24), oxygen-consuming systems to search may or may not be fruitful. 19. Margulis, L. (1996). Archaeal–eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. regenerate NAD+ for glycolysis, hence to William Martin Proc Natl Acad Sci USA 93, 1071–1076. maintain redox balance, have also been 20. Martin, W. & Müller, M. (1998). The hydrogen reported (4, 17). Of course, oxygen also has Institute of , University of hypothesis for the first eukaryote. Nature 392, 37–41. important roles in eukaryotic fatty acid and 21. Martin, W. & Schnarrenberger, C. (1997). The Düsseldorf, Universitätsstr. 1, 40225 evolution of the Calvin cycle from prokaryotic to sterol biosynthesis, but traditional formula- Düsseldorf, Germany eukaryotic chromosomes: A case study of functional tions of the endosymbiont hypothesis are at a redundancy in ancient pathways through endosymbiosis. loss to explain why eukaryotes (also amito- For correspondence. Tel: +49 211 811 3011. Curr Genet 32, 1–18. chondriate ones) possess eubacterial rather Fax: +49 211 811 3554. e-mail: 22. Mereschkowsky, C. (1905). Über Natur und Ursprung [email protected] der Chromatophoren im Pflanzenreiche. Biol Zentbl 25, than archaebacterial lipids in the first place, 593–604. English translation in Martin, W. & Kowallik, whereas the hydrogen hypothesis directly 1. Akhmanova, A., Voncken, F., van Alen, T., van Hoek, K. V. (1999), Eur J Phycol 34, 287–295. accounts for this finding as well (20). Clearly, A., Boxma, B., Vogels, G. D., Veenhuis, M. & Hackstein, 23. Müller, M. (1993). The hydrogenosome. J Gen more work is needed on the evolution and J. H. P. (1998). A hydrogenosome with a genome. Nature Microbiol 139, 2879–2889. 396, 527–528. 24. Müller, M. (1998). Enzymes and compartmentation metabolism of eukaryotes that can grow with 2. Andersson, S. G. E. & Kurland, C. G. (1999). Origins of core energy metabolism of anaerobic protists – a little or no oxygen. of mitochondria and hydrogenosomes. Curr Opin special case in eukaryotic evolution? In Evolutionary The hydrogen hypothesis invokes the Microbiol 2, 535–541. Relationships Among Protozoa, pp. 109–132. Edited by observable phenomenon of anaerobic 3. Blackstone, N. (1995). A units-of-evolution perspective G. H. Coombs, K. Vickermann, M. A. Sleigh & A. on the endosymbiont theory of the origin of the Warren. London: Chapman Hall. syntrophy (one organism gleaning a living mitochondrion. Evolution 49, 785–796. 25. Müller, M. & Martin, W. (1999). The genome of from the waste products of the 4. Brown, D. 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of another) to infer how the patterns H2O producing NADH oxidase from the protozoan of mitochondria and hydrogenosomes. BioEssays 21, of compartmentalized energy metabolism parasite . Eur J Biochem 241, 377–381. 155–161. 26. Sandman, K., Periera, S. L. & Reeve, J. N. (1998). observed among contemporary eukaryotes 5. Brown, J. R. & Doolittle, W. F. (1997). and Diversity of prokaryotic chromosomal proteins and the might have come to be. It can readily account the prokaryote-to-eukaryote transition. Microbiol Mol origin of the nucleosome. Cell Mol Life Sci 54, for a number of observations, including the Biol Rev 61, 456–502. 1350–1364. mitochondrial remnant recently described in 6. Cavalier-Smith, T. (1987). Eukaryotes with no 27. Tielens, A. G. M. & Van Hellemond, J. J. (1998). mitochondria. Nature 326, 332–333. The in anaerobically Entamoeba histolytica (28), an organism that 7. Clayton, C. E. & Michels, P. A. M. (1996). Metabolic functioning eukaryotes. Biochim Biophys Acta 1365, uses a homologue of hydrogenosomal PFO in compartmentation in African trypanosomatids. Parasitol 71–78. its cytosol (13) for ATP synthesis (24). The Today 12, 465–471. 28. Tovar, J., Fischer, A. & Clark, C. G. (1999) The syntrophy hypothesis (18) also invokes the 8. Doolittle, W. F. (1997). Fun with genealogy. Proc Natl , a novel organelle related to mitochondria in Acad Sci USA 94, 12751–12753. the amitochondrial parasite Entamoeba histolytica. Mol principle of anaerobic syntrophy, but derives a 9. Doolittle, W. F. (1998). A paradigm gets shifty. Nature Microbiol 32, 1013–1021. heterotrophic, primitively amitochondriate 392, 15–16. 29. Van Hellemond, J. J., Opperdoes, F. R. & Tielens, A. eukaryotic host and does not address the origin 10. Embley, T. M. & Hirt, R. P. (1998). Early branching G. M. (1998). Trypanosomatidae produce acetate via a of hydrogenosomes or their relationship to eukaryotes? Curr Opin Genet Dev 8, 624–629. mitochondrial acetate:succinate CoA transferase. Proc 11. Gray, M. W. & Doolittle, W. F. (1982). Has the Natl Acad Sci USA 95, 3036–3041. mitochondria. That the hydrogenosomes of endosymbiont hypothesis been proven? Microbiol Rev 30. Wallin, I. E. (1927). Symbionticism and the Origin of the ciliate Nyctotherus (1) possess a remnant 46, 1–42. Species. London: Baillière, Tindall and Cox.

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