Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The hydrogen hypothesis for the first eukaryote

Abstract

A new hypothesis for the origin of eukaryotic cells is proposed, based on the comparative biochemistry of energy metabolism. Eukaryotes are suggested to have arisen through symbiotic association of an anaerobic, strictly hydrogen-dependent, strictly autotrophic archaebacterium (the host) with a eubacterium (the symbiont) that was able to respire, but generated molecular hydrogen as a waste product of anaerobic heterotrophic metabolism. The host's dependence upon molecular hydrogen produced by the symbiont is put forward as the selective principle that forged the common ancestor of eukaryotic cells.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Schematic summary of forms of energy metabolism among heterotrophic eukaryotes (see refs 18 and19for details).
Figure 2: Hypothetical model to derive the ancestral state of eukaryotic energy metabolism put forward here, invoking strict dependence of the host upon waste products of the symbiont's anaerobic heterotrophy (see text).

References

  1. 1

    Müller, M. The hydrogenosome. J. Gen. Microbiol. 139, 2879–2889 (1993).

    Article  Google Scholar 

  2. 2

    Cavalier-Smith, T. Eukaryotes with no mitochondria. Nature 326, 332–333 (1987).

    ADS  CAS  Article  Google Scholar 

  3. 3

    Sogin, M. L., Silberman, J. D., Hinkle, G. & Morrison, H. G. Problems with molecular diversity in the Eukarya. Symp. Soc. Gen. Microbiol. 54, 167–184 (1996).

    Google Scholar 

  4. 4

    Whatley, J. M., John, P. & Whatley, F. R. From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc. R. Soc. Lond. B 204, 165–187 (1979).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Gray, M. W. & Doolittle, W. F. Has the endosymbiont hypothesis been proven? Microbiol. Rev. 46, 1–42 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Cavalier-Smith, T. The origin of eukaryote and archaebacterial cells. Ann. NY Acad. Sci. 503, 7–54 (1987).

    ADS  Google Scholar 

  7. 7

    Cavalier-Smith, T. & Chao, E. E. Molecular phylogeny of the free-living archaezoan Trepomonas agilis and the nature of the first eukaryote. J. Mol. Evol. 43, 551–562 (1996).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Zillig, W. et al. Did eukaryotes originate by a fusion event? Endocytobiosis Cell Res. 6, 1–25 (1989).

    Google Scholar 

  9. 9

    Gupta, R. S. & Golding, G. B. The origin of the eukaryotic cell. Trends Biochem. Sci. 21, 166–171 (1996).

    CAS  Article  Google Scholar 

  10. 10

    Lake, J. A. & Rivera, M. C. Was the nucleus the first endosymbiont? Proc. Natl Acad. Sci. USA 91, 2880–2881 (1994).

    ADS  CAS  Article  Google Scholar 

  11. 11

    Clark, C. G. & Roger, A. J. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl Acad. Sci. USA 92, 6518–6521 (1995).

    ADS  CAS  Article  Google Scholar 

  12. 12

    Henze, K. et al. Anuclear gene of eubacterial origin in Euglena reflects cryptic endosymbioses during protist evolution. Proc. Natl Acad. Sci. USA 92, 9122–9126 (1995).

    ADS  CAS  Article  Google Scholar 

  13. 13

    Keeling, P. W. & Doolittle, W. F. Evidence that eukaryotic triosephosphate isomerase is of alpha-proteobacterial origin. Proc. Natl Acad. Sci. USA 94, 1270–1275 (1997).

    ADS  CAS  Article  Google Scholar 

  14. 14

    Doolittle, W. F. Some aspects of the biology of cells and their possible evolutionary significance. Symp. Soc. Gen. Microbiol. 54, 1–21 (1996).

    Google Scholar 

  15. 15

    Rosenthal, B. et al. Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J. Bacteriol. 179, 3736–3745 (1997).

    CAS  Article  Google Scholar 

  16. 16

    Searcy, D. G. in The Origin and Evolution of the Cell (eds Hartman, H. & Matsuno, K.) 47–78 (World Scientific, Singapore, (1992)).

    Google Scholar 

  17. 17

    de Duve, C. Blueprint for a Cell: the Nature and Origin of Life (Patterson, Burlington, NC, (1991)).

    Google Scholar 

  18. 18

    Coombs, G. H. & Müller, M. in Biochemistry and Molecular Biology of Parasites (eds Marr, J. J. & Müller, M.) 33–47 (Academic, London, (1995)).

    Google Scholar 

  19. 19

    Müller, M. in Evolutionary Relationships Among Protozoa (eds Coombs, G. H., Vickermann, K., Sleigh, M. A. & Warren, A.) 109–132 (Chapman Hall, London, (1998)).

    Google Scholar 

  20. 20

    Müller, M. Energy metabolism of protozoa without mitochondria. Annu. Rev. Microbiol. 42, 465–488 (1988).

    Article  Google Scholar 

  21. 21

    Müller, M. in Christian Gottfried Ehrenberg-Festschrift anla¨ßlich der 14. Wissenschaftlichen Jahrestagung der Deutschen Gesellschaft für Protozoologie, 9.-11. Marz 1995 in Delitzsch (Sachsen) (eds Schlegel, M. & Hausmann, K.) 63–76 (Leipziger Universitätsverlag, Leipzig, (1996)).

    Google Scholar 

  22. 22

    Iwabe, N., Kuma, K.-I., Hasegawa, M., Osawa, S. & Miyata, T. Evolutionary relationship of archaebacteria, eubacteria and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Natl Acad. Sci. USA 86, 9355–9359 (1989).

    ADS  CAS  Article  Google Scholar 

  23. 23

    Woese, C., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria and Eukarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).

    ADS  CAS  Article  Google Scholar 

  24. 24

    Langer, D., Hain, J., Thuriaux, P. & Zillig, W. Transcription in Archaea: similarity to that in Eukarya. Proc. Natl Acad. Sci. USA 92, 5768–5772 (1995).

    ADS  CAS  Article  Google Scholar 

  25. 25

    Yamamoto, A., Hashimoto, T., Asaga, E., Hasegawa, M. & Goto, N. Phylogenetic position of the mitochondrion-lacking protozoan Trichomonas tenax, based on amino acid sequences of elongation factors 1-α and 2. J. Mol. Evol. 44, 98–105 (1997).

    ADS  CAS  Article  Google Scholar 

  26. 26

    Horner, D. S., Hirt, R. P., Kilvington, S., Lloyd, D. & Embley, T. M. Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc. R. Soc. Lond. B 263, 1053–1059 (1996).

    ADS  CAS  Article  Google Scholar 

  27. 27

    Bui, E. T. N., Bradley, P. J. & Johnson, P. J. Acommon evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl Acad. Sci. USA 93, 9651–9656 (1996).

    ADS  CAS  Article  Google Scholar 

  28. 28

    Germot, A., Philippe, H. & Le Guyader, H. Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc. Natl Acad. Sci. USA 93, 14614–14617 (1996).

    ADS  CAS  Article  Google Scholar 

  29. 29

    Roger, A. J., Clark, C. G. & Doolittle, W. F. Apossible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proc. Natl Acad. Sci. USA 93, 14618–14622 (1996).

    ADS  CAS  Article  Google Scholar 

  30. 30

    Hrdý, I. & Müller, M. Primary structure and eubacterial relationships of the pyruvate : ferredoxin oxidoreductase of the amitochondriate eukaryote, Trichomonas vaginalis. J. Mol. Evol. 41, 388–396 (1995).

    ADS  Article  Google Scholar 

  31. 31

    Blattner, F. R. et al. The complete genome sequence of Escherichia coli K-12. Science 277, 1453–1474 (1997).

    CAS  Article  Google Scholar 

  32. 32

    Kaneko, T. et al. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3, 109–136 (1996).

    CAS  Article  Google Scholar 

  33. 33

    Sánchez, L. B. & Müller, M. Purification and characterization of the acetate forming enzyme, acetyl-CoA synthetase (ADP-forming) from the amitochondriate protist, Giardia lamblia. FEBS Lett. 378, 240–244 (1996).

    Article  Google Scholar 

  34. 34

    Schönheit, P. & Schäfer, T. Metabolism of hyperthermophiles. World. J. Microbiol. Biotechnol. 11, 26–57 (1995).

    Article  Google Scholar 

  35. 35

    Markoŝ, A., Miretsky, A. & Müller, M. Aglyceraldehyde-3-phosphate dehydrogenase with eubacterial features in the amitochondriate eukaryote Trichomonas vaginalis. J. Mol. Evol. 37, 631–643 (1993).

    ADS  Article  Google Scholar 

  36. 36

    Martin, W. & Schnarrenberger, C. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32, 1–18 (1997).

    CAS  Article  Google Scholar 

  37. 37

    Fenchel, T. & Finlay, B. J. Ecology and Evolution in Anoxic Worlds (Oxford Univ. Press, Oxford, (1995)).

    Google Scholar 

  38. 38

    Gibson, J. L. & Tabita, F. R. The molecular regulation of the reductive pentose phosphate pathway in proteobacteria and cyanobacteria. Arch. Microbiol. 166, 141–150 (1996).

    CAS  Article  Google Scholar 

  39. 39

    Murrel, J. C. Genetics and molecular biology of methanotrophs. FEMS Microbiol. Lett. 88, 233–248 (1992).

    Article  Google Scholar 

  40. 40

    Thauer, R. K., Hedderich, R. & Fischer, R. in Methanogenesis: Ecology, Physiology, Biochemistry and Genetics (ed. Ferry, J. G.) 209–252 (Chapman & Hall, New York, (1993)).

    Google Scholar 

  41. 41

    Conrad, R. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2, and NO). Microbiol. Rev. 60, 609–640 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42

    Bryant, M. P., Wolin, E. A., Wolin, M. J. & Wolfe, R. S. Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch. Microbiol. 59, 20–31 (1967).

    CAS  Google Scholar 

  43. 43

    Broers, C. A. M., Stumm, C. K., Vogels, G. D. & Brugerolle, G. Psalteriomonas lanterna gen. nov., sp. nov., a free living amoboflagellate isolated from freshwater anaerobic sediments. Eur. J. Protistol. 25, 369–380 (1990).

    CAS  Article  Google Scholar 

  44. 44

    Embley, T. M. et al. Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc. R. Soc. Lond. B 262, 87–93 (1995).

    ADS  CAS  Article  Google Scholar 

  45. 45

    Finlay, kB. J., Embley, T. M. & Fenchel, T. Anew polymorphic methanogen, closely related to Methanocorpusculum parvum, living in stable symbiosis within the anaerobic ciliate Trimyema sp. J. Gen. Microbiol. 139, 371–378 (1993).

    CAS  Article  Google Scholar 

  46. 46

    Stevens, T. O. & McKinley, J. P. Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270, 450–454 (1995).

    ADS  CAS  Article  Google Scholar 

  47. 47

    Brinkmann, H. & Martin, W. Higher plant chloroplast and cytosolic 3-phosphoglycerate kinases: a case of endosymbiotic gene replacement. Plant. Mol. Biol. 30, 65–75 (1996).

    CAS  Article  Google Scholar 

  48. 48

    Kasting, J. F. Earth's early atmosphere. Science 259, 920–926 (1993).

    ADS  CAS  Article  Google Scholar 

  49. 49

    Poole, A. M., Jeffares, D. C. & Penny, D. The path from the RNA world. J. Mol. Evol. 46, 1–17 (1998).

    ADS  CAS  Article  Google Scholar 

  50. 50

    Rospert, S. et al. Methyl-coenzyme M reductase and other enzymes involved in methanogenesis from CO2and H2in the extreme thermophile Methanopyrus kandleri. Arch. Microbiol. 156, 49–55 (1991).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank H. Brinkmann, M. Embley, K. Henze, R. Herrmann, R. Hensel, D.Oesterheld and L. Sánchez for critical comments on the manuscript and gratefully acknowledge financial support from the Deutsche Forschungsgemeinschaft (W.M.) and the National Institutes of Health (M.M.).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to William Martin or Miklós Müller.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Martin, W., Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41 (1998). https://doi.org/10.1038/32096

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing