Ever since the elucidation of the main structural and functional features of eukaryotic cells and subsequent discovery of the endosymbiotic origin of mitochondria and plastids, two opposing hypotheses have been proposed to account for the origin of eukaryotic cells. One hypothesis postulates that the main features of these cells, including their ability to capture food by endocytosis and to digest it intracellularly, were developed first, and later had a key role in the adoption of endosymbionts; the other proposes that the transformation was triggered by an interaction between two typical prokaryotic cells, one of which became the host and the other the endosymbiont. Re-examination of this question in the light of cell-biological and phylogenetic data leads to the conclusion that the first model is more likely to be the correct one.
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This paper could not have been written without the invaluable help of many knowledgeable colleagues. In New York, I have benefited greatly from the advice of two former collaborators, M. Müller, who, with D. Lindmark, discovered hydrogenosomes in my laboratory, and P. Lazarow, who pioneered peroxisome biogenesis. In Brussels, my Dutch colleagues F. Opperdoes, who discovered glycosomes in the laboratory of P. Borst, and his associate P. Michels have provided many pertinent critical comments, useful suggestions and efficient help in searching the recent literature. My grateful thanks go also to T. Gabaldon for an enlightening discussion of his latest results on the phylogeny of peroxisomes and many valuable observations. I am also deeply indebted to two reviewers for their valuable criticisms. I am particularly grateful to T. Cavalier-Smith, who has allowed his identity to be revealed and has greatly helped me by putting his immense scholarship to my disposal. Finally, I express my feelings of appreciation to my friend N. Patterson for having taken time from his heavy schedule to go over my manuscript with his customary editorial care. Needless to say, I have not always followed the advice I have been given and remain solely responsible for the contents of this Essay.
The author declares no competing financial interests.
Archaebacteria are one of the two main groups of prokaryotes (the other being Eubacteria). Thus named because, when discovered, they were believed to be particularly ancient (Greek Archaios), which is no longer unanimously accepted; they share a number of special genetic and metabolic characteristics and have ether lipids in their membranes. They include many extremophiles, microbes adapted to extreme environments.
The uptake of extracellular materials by cells. The plasma membrane invaginates and vesicles pinch off that contain trapped extracellular materials enclosed within the membrane patch derived from the plasma membrane. Those vesicles, called endosomes, either fuse with lysosomes, within which their contents are digested, or migrate to a distant site, where they fuse with the plasma membrane by exocytosis, discharging their contents outside the cell (vesicular transport).
An intracellular organism that contributes to the survival of the host cell and depends on the host for its own persistence. The relationship can be either mutualistic (in which both species benefit) or commensalistic (in which one species benefits, whereas the other is not affected). Some organelles (mitochondria, plastids) are derived from degnerate endosymbionts.
Eubacteria are one of the two main groups of prokaryotes (the other being Archaebacteria). They share a number of special genetic and metabolic characteristics and have ester lipids in their membranes. They comprise all the commonly known bacteria, including those responsible for diseases.
A process by which the surrounding membrane of an intracellular vesicle fuses with the plasma membrane, so that the contents of the vesicle (usually secretory products) are discharged into the extracellular membrane.
Dependence on organic foodstuffs for survival, as opposed to autotrophy, which describes self-sufficiency, the ability to survive on mineral foodstuffs.
- Lateral gene transfer
Horizontal transfer of genes between unrelated species, as opposed to vertical inheritance within a species.
A form of endocytosis whereby large particles are taken up.
A form of endocytosis whereby droplets of fluid and soluble molecules are taken up.
A large and diverse class of lipids that are derived from 5-carbon isoprene units and enter into the formation of many natural substances, including cholesterol.
Unicellular eukaryotes including protozoans, slime molds and certain algae.
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de Duve, C. The origin of eukaryotes: a reappraisal. Nat Rev Genet 8, 395–403 (2007). https://doi.org/10.1038/nrg2071
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