Breaking through a phylogenetic impasse: a pair of associated archaea might have played host in the endosymbiotic origin of eukaryotes

Abstract

For over a century, the origin of eukaryotes has been a topic of intense debate among scientists. Although it has become widely accepted that organelles such as the mitochondria and chloroplasts arose via endosymbiosis, the origin of the eukaryotic nucleus remains enigmatic. Numerous models for the origin of the nucleus have been proposed over the years, many of which use endosymbiosis to explain its existence. Proposals of microbes whose ancestors may have served as either a host or a guest in various endosymbiotic scenarios abound, none of which have been able to sufficiently incorporate the cell biological as well as phylogenetic data which links these organisms to the nucleus. While it is generally agreed that eukaryotic nuclei share more features in common with archaea rather than with bacteria, different studies have identified either one or the other of the two major groups of archaea as potential ancestors, leading to somewhat of a stalemate. This paper seeks to resolve this impasse by presenting evidence that not just one, but a pair of archaea might have served as host to the bacterial ancestor of the mitochondria. This pair may have consisted of ancestors of both Ignicoccus hospitalis as well as its ectosymbiont/ectoparasite 'Nanoarchaeum equitans'.

Figure 1

Different phylogenetic trees describing the relationship between eukaryotes and archaea.A) Three Sisters Tree- the three domains of life are nearly equally related, with no special relationship between Eukarya and Archaea. Although a trivergence is not allowed in phylogeny, one is shown here since it would be unclear in this model which domain diverged from the others first. B) Crenote Tree- (aka Eocyte Tree) Eukarya and Crenarchaeota are sister groups. C) Euryote Tree- Eukarya and Euryarchaeota are sister groups. D) Synote Tree- Eukarya are derived from a fusion between Crenarchaeota and Euryarchaeota. For simplicity, the genetic contributions arising from the α-proteobacteria endosymbiont are not included in any of these trees.

Figure 2

Phylogeny of the Archaea based on ribosomal proteins. Unrooted Bayesian tree of the archaeal domain based on the concatenation of 57 ribosomal proteins, including established phyla (−ota), major orders (−ales), as well as the two classes of methanogens. Figure based on reference 34.