Asgard archaea illuminate the origin of eukaryotic cellular complexity

Abstract

The origin and cellular complexity of eukaryotes represent a major enigma in biology. Current data support scenarios in which an archaeal host cell and an alphaproteobacterial (mitochondrial) endosymbiont merged together, resulting in the first eukaryotic cell. The host cell is related to Lokiarchaeota, an archaeal phylum with many eukaryotic features. The emergence of the structural complexity that characterizes eukaryotic cells remains unclear. Here we describe the 'Asgard' superphylum, a group of uncultivated archaea that, as well as Lokiarchaeota, includes Thor-, Odin- and Heimdallarchaeota. Asgard archaea affiliate with eukaryotes in phylogenomic analyses, and their genomes are enriched for proteins formerly considered specific to eukaryotes. Notably, thorarchaeal genomes encode several homologues of eukaryotic membrane-trafficking machinery components, including Sec23/24 and TRAPP domains. Furthermore, we identify thorarchaeal proteins with similar features to eukaryotic coat proteins involved in vesicle biogenesis. Our results expand the known repertoire of 'eukaryote-specific' proteins in Archaea, indicating that the archaeal host cell already contained many key components that govern eukaryotic cellular complexity.

Integrative modeling of gene and genome evolution roots the archaeal tree of life

“…Although the Lokiarchaeum root could not be rejected in the reduced analysis, it was rejected by the full dataset, and it is not supported by our outgroup rooting analysis (SI Appendix, Fig. S13) or by published phylogenetic and comparative genomic analyses that group Lokiarchaeum with other "Asgard" Archaea within the TACK lineage (6,7,71). None of our analyses based on patterns of gene DTL provided any support for a root within a paraphyletic Euryarchaeota (10, 18).…”

“…In addition to the classically defined Euryarchaeota and Crenarchaeota (1), the scope of archaeal diversity has been dramatically expanded in recent years by the discovery of major new lineages using traditional and molecular methods. These lineages are of major ecological and evolutionary significance and include the Thaumarchaeota (2, 3), ammonia oxidizers found in soils and the open ocean, where they play a critical role in the global nitrogen cycle (3); the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaea) Archaea, a diverse group with small cells and genomes, whose reduced metabolic repertoires suggest that they may be symbionts or parasites of other prokaryotes (4,5); and the "Asgard" Archaea, the closest archaeal relatives of eukaryotes described to date (6,7), whose phylogenetic position and gene content are key to ongoing debates about eukaryote origins. In recent years, phylogenetic analyses have supported a clade uniting the Thaumarchaeota, Crenarchaeota, Aigarchaeota, and Korarchaeota that has been informally named the "TACK" Archaea (8) or "Proteoarchaeota" (9).…”

Evolution of peroxisomes illustrates symbiogenesis

“…Recent studies with reconstituted archaeal genomes [52,53] have allowed the discovery of new phyla of Archaea. These are more closely related to the host in the merger of archaeon and bacterium at the basis of the eukaryotic tree than ever found before.…”

Mind the gaps in cellular evolution

“…However, gaps in the cellular family tree mean that limited evidence exists that might illuminate how some eukaryote-specific features arose during the earliest intermediate steps in the evolution of eukaryotic cells. In a paper online in Nature, Zaremba-Niedzwiedzka et al 2 identify a superphylum branch of the prokaryotic family tree that contains some genes previously thought to be eukaryote-specific.…”

“…However, many aspects of the early evolution of eukaryotic cells remain unknown, such as how eukaryotic-specific features might have arisen. Zaremba-Niedzwiedzka et al 2 analysed genomic sequences from deepsea organisms which they used to identify a superphylum of Archaea that they named the Asgard group. Their genetic analysis placed this group near to the eukaryotic cell lineage.…”