Archaeal Histone Contributions to the Origin of Eukaryotes

Abstract

The eukaryotic lineage arose from bacterial and archaeal cells that underwent a symbiotic merger. At the origin of the eukaryote lineage, the bacterial partner contributed genes, metabolic energy, and the building blocks of the endomembrane system. What did the archaeal partner donate that made the eukaryotic experiment a success? The archaeal partner provided the potential for complex information processing. Archaeal histones were crucial in that regard by providing the basic functional unit with which eukaryotes organize DNA into nucleosomes, exert epigenetic control of gene expression, transcribe genes with CCAAT-box promoters, and a manifest cell cycle with condensed chromosomes. While mitochondrial energy lifted energetic constraints on eukaryotic protein production, histone-based chromatin organization paved the path to eukaryotic genome complexity, a critical hurdle en route to the evolution of complex cells. Eukaryotes from Prokaryotes: Symbiotic Contributions HighlightsThe last common ancestor of eukaryotes had mitochondria, pointing to hostsymbiont interactions at eukaryote origin. Mitochondria contributed energy, genes, and membranes to the eukaryotic lineage. What did the archaeal host contribute?Recent metagenomic studies propose that close relatives of the archaeal host exist that are 'complex' (phagocytosing) and that the archaeal host brought that complexity to eukaryotes.Yet complex archaea have not been found, and there are doubts that the metagenomic archaeal data represent truly complex archaea.Alternatively, histones could have been the key archaeal contribution to eukaryote complexity.In eukaryotes, histone modifications link gene expression to the physiological state of the cell via carbon-, energy-, and nitrogen-sensing through regulators such as AMPK, GCN2, and TOR. The Archaeal ContributionSince their discovery, archaea have been implicated as relatives of the host lineage at the origin of eukaryogenesis and mitochondria [18,19]. There is now much discussion about the possibility that complex, phagocytosing archaea might be yet discovered in nature, based on metagenomic data [20][21][22]. In that view, the contribution of archaea is unequivocal: the archaeal host brought preformed complexity to the eukaryotic lineage. Indeed, the possibility that some archaea or archaeal relatives might possess a primitive cytoskeleton has been discussed for decades [23][24][25][26].

Histone variants in archaea and the evolution of combinatorial chromatin complexity

“…Our results suggests that the last common ancestor of eukaryotes, which emerged from within the Archaea (Eme et al 2017;Williams et al 2020), might have inherited histone-based chromatin of considerable combinatorial complexity from its archaeal ancestor, with implications for the contribution of histones to the establishment of eukaryotes (Brunk and Martin 2019).…”

Isolation of an archaeon at the prokaryote-eukaryote interface

“…The evolutionary relationship between archaea and eukaryotes has been under debate, hinging on the incompleteness and contamination associated with metagenome-derived genomes and variation in results depending on tree construction protocols 20–23 . By isolating strain MK-D1, we were able to obtain a closed genome (Supplementary Table S1 and Fig.…”

Bacterial genes outnumber archaeal genes in eukaryotic genomes

“…Schematic representation of eukaryote origin involving an archaeal host and a mitochondrial symbiont that transforms the host via gene transfer from the endosymbiont [21,43]. The model combines elements of different proposals: bacterial outer membrane vesicles at the origin of the eukaryotic endomembrane system [4]; archaeal outer membrane vesicles at the origin of host membrane protrusions enabling endosymbiosis without phagocytosis [21]; a syncytial eukaryote common ancestor [56]; eukaryote origin starting an archaeal host and a bacterial symbiont brought into physical symbiotic interaction by anaerobic syntrophic interactions [21,43]; a combination of information (host) plus metabolism and energy (symbiont) [26,34] at eukaryote origin.…”

“…A symbiogenic origin of eukaryotes would run counter to one of the key goals of phylogenetics, namely to place eukaryotes in a natural system of phylogenetic classification where all groups are named according to their position in a bifurcating tree. If eukaryotes arose via symbiosis of an archaeon (the host) and a bacterium (the mitochondrion), then eukaryotes would reside simultaneously on both the archaeal and the bacterial branches in phylogenetic schemes [26,27], whereby plants and algae that stem from secondary symbioses [28] would reside on recurrently anastomosing branches as in Fig. 1d.…”