Abstract
The archaeal ancestor scenario (AAS) for the origin of eukaryotes implies the emergence of a new kind of organism from the fusion of ancestral archaeal and bacterial cells. Equipped with this “chimeric” molecular arsenal, the resulting cell would gradually accumulate unique genes and develop the complex molecular machineries and cellular compartments that are hallmarks of modern eukaryotes. In this regard, proteins related to phagocytosis and cell movement should be present in the archaeal ancestor, thus identifying the recently described candidate archaeal phylum “Lokiarchaeota” as resembling a possible candidate ancestor of eukaryotes. Despite its appeal, AAS seems incompatible with the genomic, molecular, and biochemical differences that exist between Archaea and Eukarya. In particular, the distribution of conserved protein domain structures in the proteomes of cellular organisms and viruses appears hard to reconcile with the AAS. In addition, concerns related to taxon and character sampling, presupposing bacterial outgroups in phylogenies, and nonuniform effects of protein domain structure rearrangement and gain/loss in concatenated alignments of protein sequences cast further doubt on AAS-supporting phylogenies. Here, we evaluate AAS against the traditional “three-domain” world of cellular organisms and propose that the discovery of Lokiarchaeota could be better reconciled under the latter view, especially in light of several additional biological and technical considerations.
Highlights
The discovery of the novel candidate archaeal phylum “Lokiarchaeota” from metagenomic samples taken from sites near Loki’s Castle hydrothermal vents of the Arctic Ocean was recently reported [1]
Archaea-like genes in eukaryotes can be explained under the Woesian 3D scenario by invoking a sister group relationship between Archaea and Eukarya, a view historically supported by phylogenies rooted with many paralogous gene sequences [18, 19]
Even ignoring evidence from FSF distributions, alternative explanations can account for the purported chimerism that is at the root of archaeal ancestor scenario (AAS) models suggesting that chimerism could be an oversimplified interpretation of eukaryotic genomes
Summary
The discovery of the novel candidate archaeal phylum “Lokiarchaeota” from metagenomic samples taken from sites near Loki’s Castle hydrothermal vents of the Arctic Ocean was recently reported [1]. The approach is susceptible to heterotachy (i.e., unequal evolutionary rates among genes in a concatenated set) [35, 36], which can complicate inferring deep evolutionary relationships and can introduce distortions to interdomain calculations, among other issues (see Section 5) In light of these considerations, here we examine the evidence supporting the 2D scenario for the diversification of cellular life, perform taxa and character manipulations to reanalyze the dataset of Spang et al [1] that supported the Lokiarchaeota-Eukarya sisterhood, and consider several biological and technical issues that weaken the 2D in favor of the 3D ToL. Under AAS, this new partner must invade the eukaryotic genome (or originate de novo) after the proposed fusion event because eukaryotic RNA and retrotranscribing virus families have hitherto not been described in Archaea (see Figure 1 in [41]) This poses a conceptual problem because modern RNA viruses are likely relics of ancient RNA viruses that played significant roles in evolutionary history, perhaps even contributing to the discovery of DNA [42]. It rather underestimates the distinctive and global nature of eukaryotic genomes
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