ARCHAEAL EVOLUTION Evolutionary Insights from the Vikings

RESEARCH HIGHLIGHTS

Nature Reviews Microbiology | Published online 16 Jan 2017; doi:10.1038/nrmicro.2016.198

ARCHAEAL EVOLUTION Evolutionary insights from the Vikings

The emergence of the eukaryotic cell ASGARD — after the invisible the closest known homologue of during evolution gave rise to all com- ‘Gods of Asgard’ in Norse mythology. eukaryotic epsilon DNA polymerases primordial plex life forms on Earth, including The superphylum consists of the identified thus far. eukaryotic multicellular organisms such as ani- previously identified Lokiarchaeota Members of the ASGARD super- mals, plants and fungi. However, the and Thorarchaeota phyla, and the phylum were particularly enriched vesicular and origin of eukaryotes and their char- newly identified Odinarchaeota and for eukaryotic signature proteins trafficking acteristic structural complexity has Heimdallarchaeota phyla. Using that are involved in intracellular components remained a mystery. The most recent phylogenomics, they discovered trafficking and secretion. Several are derived insights into eukaryogenesis support a strong phylogenetic association proteins contained domain signatures the endosymbiotic theory, which between ASGARD lineages and of eukaryotic transport protein from our proposes that the first eukaryotic eukaryotes that placed the eukaryote particle (TRAPP) complexes, which archaeal cell arose from archaea through the lineage in close proximity to the are involved in transport from the ancestor acquisition of an alphaproteobacterial ASGARD superphylum. endoplasmic reticulum through endosymbiont. Using phylogenomic Next, to investigate the emergence the Golgi apparatus in eukaryotes. In analyses of uncultivated archaeal lin- of eukaryotic gene content in the addition, eukaryotic homologues of eages, Zaremba-Niedzwiedzka et al. ASGARD lineages, the authors the Sec23/24 family that are compo- provide biological insights into the searched for the presence of proteins nents of the COPII vesicle coatomer archaeal ancestor of eukaryotes and that are unique to eukaryotes (eukary protein complex were found in the the primal stages of eukaryogenesis. otic signature proteins) and found Thorarchaeota, which prompted the First, the authors identified and that ASGARD lineages were enriched authors to search for further eukar- characterized phyla that are closely for these proteins. For example, yotic coatomer proteins. Eukaryotic related to the archaeal phylum homologues of eukaryotic endosomal coatomer proteins are composed of Lokiarchaeota. Previous studies had sorting complex required for trans- amino-terminal β-propeller folds placed the Lokiarchaeota as the most port (ESCRT) systems, ubiquitylation followed by a carboxy-terminal closely related archaea to eukaryotes proteins and orthologues of essential α-solenoid fold; both of these folded as they have genes that are typically eukaryotic cytoskeletal components domains are extremely rare in prokary associated with eukaryotic functions, were enriched. Indeed, several key otic proteins. Remarkably, the authors such as membrane remodelling. The eukaryotic cytoskeletal proteins identified further eukaryotic-like authors identified two additional including tubulin, gelsolin-domain coatomer proteins in the ASGARD related phyla that they grouped and profilin-domain proteins, and superphylum, including proteins into a superphylum and named homologues of the actin-related that contain both β-propeller and protein 2/3 (ARP2/3) complex were α-solenoid folds, which indicates that identified, which indicates that mem- primordial eukaryotic vesicular and bers of the ASGARD superphylum trafficking components are derived have several fundamental building from our archaeal ancestor. blocks that are required for the evolu- In sum, this study provides an tion of a sophisticated eukaryotic-like exciting new perspective on the origin cytoskeleton. Interestingly, the authors of eukaryotic membrane trafficking, also found that genes that encode eukaryogenesis and the evolution of a ESCRT and ubiquitin modifier system compartmentalized and structurally proteins were co-organized in the complex eukaryotic cell, which ulti- same gene clusters, which indicates mately led to the acquisition of new that ESCRT-mediated protein degra- cellular functions that drove the dation might operate in members of evolution of multicellular life on Earth. the ASGARD superphylum, a system Ashley York

that was only thought to exist in ORIGINAL ARTICLE Zaremba-Niedzwiedzka, K. eukaryotes. Similarly, an epsilon DNA et al. ASGARD archaea illuminate the origin of polymerase subunit was identified in eukaryotic cellular complexity. Nature http://dx. doi.org/10.1038/nature21031 (2017)

Neil Smith/Macmillan Publishers Limited the Heimdallarchaeota that represents