Unique mobile elements and scalable gene flow at the prokaryote–eukaryote boundary revealed by circularized Asgard archaea genomes

Abstract

Eukaryotic genomes are known to have garnered innovations from both archaeal and bacterial domains but the sequence of events that led to the complex gene repertoire of eukaryotes is largely unresolved. Here, through the enrichment of hydrothermal vent microorganisms, we recovered two circularized genomes of Heimdallarchaeum species that belong to an Asgard archaea clade phylogenetically closest to eukaryotes. These genomes reveal diverse mobile elements, including an integrative viral genome that bidirectionally replicates in a circular form and aloposons, transposons that encode the 5,000 amino acid-sized proteins Otus and Ephialtes. Heimdallaechaeal mobile elements have garnered various genes from bacteria and bacteriophages, likely playing a role in shuffling functions across domains. The number of archaea- and bacteria-related genes follow strikingly different scaling laws in Asgard archaea, exhibiting a genome size-dependent ratio and a functional division resembling the bacteria- and archaea-derived gene repertoire across eukaryotes. Bacterial gene import has thus likely been a continuous process unaltered by eukaryogenesis and scaled up through genome expansion. Our data further highlight the importance of viewing eukaryogenesis in a pan-Asgard context, which led to the proposal of a conceptual framework, that is, the Heimdall nucleation–decentralized innovation–hierarchical import model that accounts for the emergence of eukaryotic complexity.

Evolutionary Diversification of MethanotrophicCa. Methanophagales (ANME-1) and Their Expansive Virome

“…4a, the ANME-1 MGEs from South Pescadero Basin were primarily targeted by spacers found locally (n=1912), but also showed a high number of matches to Guaymas Basin spacers (n=894). As previously found for the Asgard archaeal mobilome 69 , the apparent frequency of cross-site spacer-mobilome mapping indicates a significant fraction of the ANME-1 mobilome has migrated across these sediment-hosted hydrothermal vent ecosystems, along with their hosts 38 .…”

Looking through the Lens of the Ribosome Biogenesis Evolutionary History: Possible Implications for Archaeal Phylogeny and Eukaryogenesis

“…Intriguingly, the tRNA Ala is located next to the 23S rRNA, in a similar fashion normally found in Euryarchaeota. To our surprise, unlinked rRNA genes are not restricted to Lokiarchaeota, as do found in Heimdallarchaeota, Wukongarchaeota, Njordarchaeota, and other recently described Asgard archaea we could examine ( Zaremba-Niedzwiedzka et al 2017 ; Liu et al 2021 ; Xie et al 2021 ; Wu et al 2022 ) (see fig. 2 C and supplementary information, Supplementary Material online).…”

“…However, it is interesting to note that both linked and unlinked rRNA genes organization in several Asgard archaea (e.g., Odin-/Loki-/Heimdallarchaeota) were identified from metagenome assembly ( Zaremba-Niedzwiedzka et al 2017 ). Moreover, the linked rRNA genes organization of Odinarchaea LCB_4 and unlinked rRNA genes organization in Heimdallarchaeota have been recently confirmed by long-read sequencing ( Tamarit et al 2021 ; Wu et al 2022 ). Finally, the unlinked rRNA genes organization observed in Wukongarchaeota, Njordarchaeota (see supplementary information, Supplementary Material online) were obtained from independent metagenomic analyses ( Liu et al 2021 ; Xie et al 2021 ).…”

Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere

“…The DPANN group (acronym referring to its first described member lineages, the Diapherotrites, Parv-, Aenigm-, Nano-, and Nanohaloarchaeota) now includes more than eight distinct archaeal phyla ( Rinke et al 2021 ) that group together with Nanoarchaeota, an archaeal clade represented by the ultrasmall and ectosymbiotic archaeon Nanoarchaeum equitans ( Huber et al 2002 ). Representatives of DPANN have small genomes and cell sizes, are characterized by restricted anabolic and catabolic capabilities, and include obligate ectosymbionts some of which have been cultivated in coculture with their hosts belonging to the Halobacteriota, Thermoproteota, and Thermoplasmatota ( Huber et al 2002 ; Podar et al 2013 ; Munson-McGee et al 2015 ; Wurch et al 2016 ; Golyshina et al 2017 ; Krause et al 2017 ; Hamm et al 2019 ; St John et al 2019 ; La Cono et al 2020 ; Sakai et al 2022 ). Indeed, symbiotic lifestyles have been suggested to represent a common feature of genome-reduced members of the DPANN ( Castelle et al 2018 ).…”