The Asgard Archaeal-Unique Contribution to Protein Families of the Eukaryotic Common Ancestor Was 0.3%

Abstract

Summary The identification of the asgard archaea has fueled speculations regarding the nature of the archaeal host in eukaryogenesis and its level of complexity prior to endosymbiosis. Here we analyzed the coding capacity of 150 eukaryotes, 1000 bacteria, and 226 archaea, including the only cultured member of the asgard archaea. Clustering methods that consistently recover endosymbiotic contributions to eukaryotic genomes, recover an asgard archaeal-unique contribution of a mere 0.3% to protein families present in the last eukaryotic common ancestor, while simultaneously suggesting that this group’s diversity rivals that of all other archaea combined. The number of homologs shared exclusively between asgard archaea and eukaryotes is only 27 on average. This tiny asgard archaeal-unique contribution to the root of eukaryotic protein families, questions claims that archaea evolved complexity prior to eukaryogenesis. Genomic and cellular complexity remains a eukaryote-specific feature and is best understood as the archaeal host’s solution to housing an endosymbiont.

Endosymbiotic selective pressure at the origin of eukaryotic cell biology

“…aminopeptidases, mTOR interacting proteins, glycosyltransferases), and a small fraction appear to originate from archaea (DNA licensing proteins of cell cycle, ARG GTPases, N -glycan biosynthesis). The distribution of protein families across prokaryotes and eukaryotes ( Figure 2 ) confirms that eukaryotes acquired genes from bacterial or archaeal sources and co-opted them to suit new eukaryotic traits evolving in the FECA to LECA transition, but the majority of protein families involved in eukaryotic cellular complexity are absent across the entire realm of prokaryotic diversity ( Brunk and Martin, 2019 ; Dell et al, 2010 ; Knopp et al, 2021 ; Liu et al, 2021 ; Lombard, 2016 ). Hence, HGT falls short at explaining the pro- to eukaryote transition with respect to the origin of thousands of eukaryote-unique gene families and a reason for their positive selection in the absence of an endosymbiont.…”

“…two domains of life, bacteria and archaea, evolved from the origin of life and eukaryotes emerged from within archaea after endosymbiosis of an alphaproteobacterial partner). (iii) They provide no evidence for the presence of bacterial-type ester-linked lipids in asgard archaea, (iv) reject a complex archaeal ancestor necessary to explain the patchy distribution of eukaryogenesis-relevant gene families ( Wu et al, 2022 ), and (v) show that the asgard archaeal set of genes before unique to eukaryotes closes the gap to the number of gene families encoded by eukaryotes by only 0.3% ( Knopp et al, 2021 ) or less ( Liu et al, 2021 ). Hence, with respect to explaining the origin of eukaryotic traits and a rationale for their universal presence in eukaryotes, the asgard archaea and their syntrophic bacterial partners support and place us at scenarios that were submitted some 25 years ago ( Martin and Müller, 1998 ; Moreira, 1998 ; Vellai and Vida, 1999 ).…”

“…Some models can be interpreted one way or the other ( Imachi et al, 2020 ), while some explicitly state that the host cell was a bona fide prokaryote and that eukaryotic traits and biology evolved after endosymbiosis ( Gould et al, 2016 ; López-García and Moreira, 2020 ; Wu et al, 2022 ). Notably, the differences among these models rest upon a few dozen genes from the pan-asgard archaeal genome repertoire, whose overall unique contribution to the roots of eukaryotes was 0.3% or less ( Knopp et al, 2021 ; Liu et al, 2021 ). Sources and timing of gene acquisition in the FECA to LECA transition are equally essential to correctly quantify as they remain hard to predict.…”

“…An autogenous origin of cellular complexity on the basis of an archaeal (host) source alone would predict the opposite but prokaryotes are characterized by mosaic genomes due to horizontal gene transfer (HGT) whose contribution to cellular complexity prior to endosymbiosis is debated ( Martin et al, 2017b ; Pittis and Gabaldón, 2016 ). Claims concerning differential loss of genes in extant archaea ( Koonin and Yutin, 2014 ; Eme et al, 2017 ) are at odds with pangenomes that support a pan-asgard concept ( Knopp et al, 2021 ; Liu et al, 2021 ). Dynamic genomes and the time passed since eukaryote origin challenge phylogenomic approaches and can skew interpretations including the timing of compartment origin.…”

Highlight: Unraveling the Origins of LUCA and LECA on the Tree of Life

“…One critical question is whether such features may have originated in the ancestral archaeal lineage prior to eukaryogenesis. Knopp et al (2021) found that only 0.3% of protein families present in LECA can be attributed to the Asgard archaea, casting doubt on the idea that the ancestral archaeal lineage evolved many of these features prior to eukaryogenesis. Investigating another aspect of LECA, Skejo et al (2021) intriguingly suggested that LECA may have been multinucleate, pointing to the commonality of multinucleated forms across eukaryotic supergroups.…”