Comparative population genomic analyses of transporters within the Asgard archaeal superphylum

Abstract

Upon discovery of the first archaeal species in the 1970s, life has been subdivided into three domains: Eukarya, Archaea, and Bacteria. However, the organization of the three-domain tree of life has been challenged following the discovery of archaeal lineages such as the TACK and Asgard superphyla. The Asgard Superphylum has emerged as the closest archaeal ancestor to eukaryotes, potentially improving our understanding of the evolution of life forms. We characterized the transportomes and their substrates within four metagenome-assembled genomes (MAGs), that is, Odin-, Thor-, Heimdall- and Loki-archaeota as well as the fully sequenced genome of Candidatus Prometheoarchaeum syntrophicum strain MK-D1 that belongs to the Loki phylum. Using the Transporter Classification Database (TCDB) as reference, candidate transporters encoded within the proteomes were identified based on sequence similarity, alignment coverage, compatibility of hydropathy profiles, TMS topologies and shared domains. Identified transport systems were compared within the Asgard superphylum as well as within dissimilar eukaryotic, archaeal and bacterial organisms. From these analyses, we infer that Asgard organisms rely mostly on the transport of substrates driven by the proton motive force (pmf), the proton electrochemical gradient which then can be used for ATP production and to drive the activities of secondary carriers. The results indicate that Asgard archaea depend heavily on the uptake of organic molecules such as lipid precursors, amino acids and their derivatives, and sugars and their derivatives. Overall, the majority of the transporters identified are more similar to prokaryotic transporters than eukaryotic systems although several instances of the reverse were documented. Taken together, the results support the previous suggestions that the Asgard superphylum includes organisms that are largely mixotrophic and anaerobic but more clearly define their metabolic potential while providing evidence regarding their relatedness to eukaryotes.

On the trail of iron uptake in ancestral Cyanobacteria on early Earth

“…The FeoB transporter functions as a Fe(II) permease, and its cytosolic G‐protein domain is considered a precursor of eukaryotic G‐proteins (Hantke, 2003). Genes putatively identified as feoB analogues are found within many Archaea genomes (Gómez‐Garzón et al, 2022; Russum et al, 2021), while pairwise analyses place FeoB in a hierarchical orthologous group that appears at the level of LUCA, with FutB, Ftr1, ZIP, NRAMP, and ExbB/D appearing later in Bacteria (Altenhoff et al, 2018). Cyanobacteria, with their high iron requirements, had to adjust to ever reducing levels of Fe(II) with increasing oxygenation (Fresenborg et al, 2020; Jiang et al, 2020; Qiu et al, 2022).…”

Two-Component System Sensor Kinases from Asgardian Archaea May Be Witnesses to Eukaryotic Cell Evolution

“…Additionally, the C. Prometheoarchaeum genome reveals a more detailed and accurate signal transduction repertoire in the Lokiarchaeum branch, whereas, in the Heimdallarchaeota branch, the homology to bacterial counterparts is limited, suggesting that it is the branching point to specialized kinases and that the preservation of kinases that can sense specific metabolites and redox states was crucial for the establishment of an endosymbiotic relationship, specifically of an oxygen-utilizing endosymbiont [ 2 ]. In particular, the presence of AtoS homologs suggests the ability to sense short-chain fatty acids [ 31 ] and may be the link between the metabolic needs of Asgardian archaea and the relationship for establishing the strong metabolic crosstalk that eventually resulted in the development of endosymbiosis, e.g., acetate perception for the regulation of acetyl coenzyme A synthesis, as described previously [ 32 ]. This is consistent with the repertoire of metabolite transporters found in the C. Prometheoarchaeum syntrophicum MK-D1 strain and other Asgardian meta-genome assemblies previously reported that indicate that these organisms depend on the transport of all the molecules they need [ 33 ].…”

Structural and biochemical evidence for the emergence of a calcium-regulated actin cytoskeleton prior to eukaryogenesis

“…This indicates that their last common ancestor will have possessed a 2DGel which responded to calcium ions. Sequence analysis has identified several potential eukaryotic-like calcium channels in Asgard archaea genomes, which have been predicted to control calcium influx into these organisms 29 . In particular, Loki, Heim and Thor contain potential Calcium Load-activation Calcium Channels (CLAC), and Loki and Heim potential presenilins 29 .…”

“…Sequence analysis has identified several potential eukaryotic-like calcium channels in Asgard archaea genomes, which have been predicted to control calcium influx into these organisms 29 . In particular, Loki, Heim and Thor contain potential Calcium Load-activation Calcium Channels (CLAC), and Loki and Heim potential presenilins 29 . Thus, Asgard archaea may use calcium channels to regulate calcium levels, and in turn, control actin dynamics.…”