Changing perspectives on the origin of eukaryotes

doi:10.1016/S0169-5347(98)01490-6

Trends in Ecology & Evolution

Volume 13, Issue 12, 1 December 1998, Pages 493-497

https://doi.org/10.1016/S0169-5347(98)01490-6 Get rights and content

Abstract

From the initial application of molecular techniques to the study of microbial organisms, three domains of life emerged, with eukaryotes and archaea as sister taxa. However, recent analyses of an expanding molecular data set reveal that the eukaryotic genome is chimeric with respect to archaea and bacteria. Moreover, there is now evidence that the primitive eukaryotic group `Archezoa' once harbored mitochondia. These discoveries have challenged the traditional stepwise model of the evolution of eukaryotes, in which the nucleus and microtubules evolve before the acquisition of mitochondria, and consequently compel a revision of existing models of the origin of eukaryotic cells.

Section snippets

Chimeric nature of eukaryotic genomes

The recent accumulation of DNA sequence data from numerous genes has made it clear that eukaryotic genomes are chimeric with respect to archaea and bacteria6, 7, 8, 9, 10. A genome is chimeric when a gene (or genes) within an organism does not simply trace the history of vertical transmission of genetic information from one generation to the next. Instead, chimeric genomes are the result of lateral transmission of genes (or genomes) across species boundaries. As a consequence of lateral gene

Changing perspectives on Archezoa

In addition to changing our views on the nature of eukaryotic genomes, we must also contend with the abandonment of the eukaryotic group `Archezoa' (not to be confused with the prokaryotic group archaea). Based on analysis of the ssu-rRNA gene2, 19, several amitochondrial taxa were shown to represent the basal lineages of eukaryotes (Fig. 1), including diplomonads (e.g. Giardia lamblia), trichomonads (e.g. Trichomonas vaginalis) and microsporidians (e.g. Vairimorpha necatrix). These

Theories on the origins of eukaryotes

Models of the origin of eukaryotic cells have focused on the evolution of the nucleus and microtubules. The data on the chimeric nature of eukaryotic genomes, combined the possibility that the acquisition of mitochondria occurred simultaneously with the emergence of eukaryotes, require that we re-evaluate these models for their ability to explain four characteristics of the last common ancestor of all extant eukaryotes: the presence of a nucleus, microtubules, mitochondria and a chimeric genome

Conclusions and perspectives

Recent data on the nature of eukaryotic genomes and the timing of the acquisition of mitochondria compel us to transform our views on the origin of eukaryotes. It is now possible to assume that the original endosymbiotic event that gave rise to the mitochondria (whether for respiration[40], hydrogen-dependent metabolism[42]or sulfur-dependent metabolism[43]) occurred in the ancestor of all extant eukaryotes, and that this endosymbiosis explains both the chimeric nature of eukaryotic genomes and

Acknowledgements

I wish to thank J.T. Bonner and D.H. Berger and three anonymous reviewers for their comments on this article. The work was supported by a grant to the Smith College Dept of Biological Sciences from the Albert F. Blakeslee Fund (administered by the National Academy of Sciences, USA).

References (48)

M Schlegel
Molecular phylogeny of eukaryotes
Trends Ecol. Evol.
(1994)
W Zillig
Comparative biochemistry of Archaea and Bacteria
Curr. Opin. Genet. Dev.
(1991)
J.P Gogarten
The early evolution of cellular life
Trends Ecol. Evol.
(1995)
G McFadden et al.
Something borrowed, something green: lateral transfer of chloroplasts by secondary endosymbiosis
Trends Ecol. Evol.
(1995)
C Zeyl et al.
Symbiotic DNA in eukaryotic genomes
Trends Ecol. Evol.
(1996)
A Germot et al.
Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae
Mol. Biochem. Parasitol.
(1997)
R.P Hirt
A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: Molecular evidence that microsporidia once contained mitochondria
Curr. Biol.
(1997)
T.M Embley et al.
Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria?
Trends Ecol. Evol.
(1997)
R.S Gupta et al.
The origin of the eukaryotic cell
Trends Biochem. Sci.
(1996)
M.L Sogin
Early evolution and the origin of eukaryotes
Curr. Opin. Genet. Dev.
(1991)

C.R Woese et al.

Phylogenetic structure of the prokaryotic domain: the primary kingdoms

Proc. Natl. Acad. Sci. U. S. A.

(1977)

M.L Sogin

Ancestral relationships of the major eukaryotic lineages

Microbiologia

(1996)

A.H Knoll

The early evolution of eukaryotes: a geological perspective

Science

(1992)

D.F Feng et al.

Determining divergence times with a protein clock: update and reevaluation

Proc. Natl. Acad. Sci. U. S. A.

(1997)

G Pühler

Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome

Proc. Natl. Acad. Sci. U. S. A.

(1989)

G.B Golding et al.

Protein-based phylogenies support a chimeric origin for the eukaryotic genome

Mol. Biol. Evol.

(1995)

J.R Brown et al.

Archaea and the prokaryote-to-eukaryote transition

Micro. Mol. Biol. Rev.

(1997)

Doolittle, W.F. (1996) Some aspects of the biology of cells and their possible evolutionary significance, in Evolution...

D.R Edgell et al.

Archaebacterial genomics: the complete genome sequence of Methanococcus jannaschii

BioEssays

(1997)

Hillis, D.M., Moritz, C. and Mable, B.K. (1996) Molecular Systematics (2nd edn),...

W.P Maddison

Gene trees in species trees

Syst. Biol.

(1997)

L.A Katz

Transkingdom transfer of the phosphoglucose isomerase gene

J. Mol. Evol.

(1996)

Gogarten, J.P., Hilario, E. and Olendzenski, L. (1996) Gene duplications and horizontal gene transfer during early...

T Cavalier-Smith et al.

Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote

J. Mol. Evol.

(1996)

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Trends in Ecology & Evolution

ReviewsChanging perspectives on the origin of eukaryotes

Abstract

Section snippets

Chimeric nature of eukaryotic genomes

Changing perspectives on Archezoa

Theories on the origins of eukaryotes

Conclusions and perspectives

Acknowledgements

Trends Ecol. Evol.

Curr. Opin. Genet. Dev.

Trends Ecol. Evol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Mol. Biochem. Parasitol.

Curr. Biol.

Trends Ecol. Evol.

Trends Biochem. Sci.

Curr. Opin. Genet. Dev.

Phylogenetic structure of the prokaryotic domain: the primary kingdoms

Proc. Natl. Acad. Sci. U. S. A.

Ancestral relationships of the major eukaryotic lineages

Microbiologia

The early evolution of eukaryotes: a geological perspective

Science

Determining divergence times with a protein clock: update and reevaluation

Proc. Natl. Acad. Sci. U. S. A.

Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome

Proc. Natl. Acad. Sci. U. S. A.

Protein-based phylogenies support a chimeric origin for the eukaryotic genome

Mol. Biol. Evol.

Archaea and the prokaryote-to-eukaryote transition

Micro. Mol. Biol. Rev.

Archaebacterial genomics: the complete genome sequence of Methanococcus jannaschii

BioEssays

Gene trees in species trees

Syst. Biol.

Transkingdom transfer of the phosphoglucose isomerase gene

J. Mol. Evol.

Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote

J. Mol. Evol.

Reviews
Changing perspectives on the origin of eukaryotes