Endosymbiotic theories for eukaryote origin

Abstract

For over 100 years, endosymbiotic theories have figured in thoughts about the differences between prokaryotic and eukaryotic cells. More than 20 different versions of endosymbiotic theory have been presented in the literature to explain the origin of eukaryotes and their mitochondria. Very few of those models account for eukaryotic anaerobes. The role of energy and the energetic constraints that prokaryotic cell organization placed on evolutionary innovation in cell history has recently come to bear on endosymbiotic theory. Only cells that possessed mitochondria had the bioenergetic means to attain eukaryotic cell complexity, which is why there are no true intermediates in the prokaryote-to-eukaryote transition. Current versions of endosymbiotic theory have it that the host was an archaeon (an archaebacterium), not a eukaryote. Hence the evolutionary history and biology of archaea increasingly comes to bear on eukaryotic origins, more than ever before. Here, we have compiled a survey of endosymbiotic theories for the origin of eukaryotes and mitochondria, and for the origin of the eukaryotic nucleus, summarizing the essentials of each and contrasting some of their predictions to the observations. A new aspect of endosymbiosis in eukaryote evolution comes into focus from these considerations: the host for the origin of plastids was a facultative anaerobe.

Keywords: anaerobes; endosymbiosis; eukaryotes; mitochondria; nucleus; plastids.

Figure 1.

Models describing the origin of the nucleus in eukaryotes. (a–o) Schematic of various models accounting for the origin of the nucleus. Archaeal cells/membranes are represented with red, while blue indicates eubacterial cells/membranes. Black membranes are used when the phylogenetic identity of the cell is not clear or not specified. See also [22,53].

Figure 2.

Models describing the origin of mitochondria and/or chloroplasts in eukaryotes. (a–q) Schematic of various models accounting for the origin of mitochondria and/or chloroplasts. Archaeal cells/membranes are represented with red, while blue indicates eubacterial cells/membranes. Black membranes are used when the identity of the cell is not clear and green is used for cyanobacterial derived cells/membranes. See also [22].

Figure 3.

Mitochondrial origin in a prokaryotic host. (a–h) Illustrations for various stages depicting the transition of a H₂-dependent archaeal host (in red) and a facultatively anaerobic α-proteobacterium (in blue) to an eukaryote. See also [25,34,35] regarding this transition, and [116,117] regarding gene transfer from organelles to the nucleus.

Figure 4.

Evolution of anaerobes and the plastid. (a–d) Diversification of the mitochondria-containing ancestor to eukaryotes containing specialized forms of the organelle, hydrogenosomes, mitosomes and anaerobic mitochondria. See also [21,143]. (e,f) Primary symbiotic origin of a plastid involving a cyanobacterium in a facultative anaerobic host (see text), followed by gene transfer to the nucleus resulting in a plastid-bearing ancestor. See also [144]. (g–i) Diversification of the plastid-bearing ancestor to glaucocystophytes, chlorophytes and rhodophytes. See also [25].