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The expanding Asgard archaea and their elusive relationships with Eukarya - PubMed

  • ️Sat Jan 01 2022

The expanding Asgard archaea and their elusive relationships with Eukarya

Violette Da Cunha et al. mLife. 2022.

Abstract

The discovery of Asgard archaea and the exploration of their diversity over the last 6 years have deeply impacted the scientific community working on eukaryogenesis, rejuvenating an intense debate on the topology of the universal tree of life (uTol). Here, we discuss how this debate is impacted by two recent publications that expand the number of Asgard lineages and eukaryotic signature proteins (ESPs). We discuss some of the main difficulties that can impair the phylogenetic reconstructions of the uTol and suggest that the debate about its topology is not settled. We notably hypothesize the existence of horizontal gene transfers between ancestral Asgards and proto-eukaryotes that could result in the observed abnormal behaviors of some Asgard ESPs and universal marker proteins. This hypothesis is relevant regardless of the scenario considered regarding eukaryogenesis. It implies that the Asgards were already diversified before the last eukaryotic common ancestor and shared the same biotopes with proto-eukaryotes. We suggest that some Asgards might be still living in symbiosis today with modern Eukarya.

Keywords: Asgard; horizontal gene transfer; molecular phylogeny; tree of life.

© 2022 The Authors. mLife published by John Wiley & Sons Australia, Ltd. on behalf of Institute of Microbiology, Chinese Academy of Sciences.

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Figures

Figure 1
Figure 1

Two vs. three domains models for the universal tree of life. In the two domains (2D) model, Eukarya (E) branch within Archaea (A) and should be formally considered to be Archaea themselves (otherwise Archaea being paraphyletic are not a valid taxon). This schematic tree is based on one possible result of Liu et al. in 2021, in which eukaryotes belong to the Asgard superphylum. In the three domains, model Archaea (A) and Eukarya (E) form a clade dubbed Arkarya (AK) in Forterre. The bacterial branch (green) is much longer than the eukaryotic and archaeal branches (blue and red, respectively). The archaeal branch (red) is very short and only present in the three domains (3D) model. This schematic tree is based on Da Cunha et al.. Eury(eury): Euryarchaeota; Cren: Crenarchaeota. TACK is the acronym for the clade grouping Thaumarchaea, Aigarchaea, Crenarchaea, and Korarchaea; DPANN is the acronym for the clade grouping Diapherotrites, Parvarchaea, Aenigmarchaea, Nanohaloarchaea, and Nanoarchaea; BAT is the acronym for the clade grouping Bathyarchaea, Aigarchaea, and Thaumarchaea. The trees are rooted in the bacterial branch, based on comparative analysis of ribosomal protein distribution.

Figure 2
Figure 2

Schematic representation of the known diversity of the Asgard archaea including the recently published lineages. In this schema, we indicate in orange and red the newly discovered lineages introduced in the two publications of Liu et al. and Xie et al., respectively, and in grey new lineages not present in these publications corresponding to the Sifarchaea, the Jordarchaeia and Asgard Lake Cootharaba. The schema was designed combining the trees of all these publications. The suffix within brackets indicates that, depending on the authors, these lineages are considered to be Phylum (ota), Families (aceae), or Orders (ales). We locate the position of LAsCA (last Asgard archaeal common ancestor) based on the root observed in most phylogenetic trees, and used by Liu et al. to discuss the ESPs distribution. For each Asgard lineage, we also indicate the year of publication of the genome of its first representative, and changes in taxonomy are indicated by color changes of the dots. The light purple dots indicate that Asgards of the Karia and Hodar and lineages were described before 2017 as Loki 2 and Loki 3, respectively. In addition, the number of genomes available for each lineage is indicated within brackets.

Figure 3
Figure 3

Two possible long branch attraction effects that could transform a 3D uTol into a 2D uTol and vice versa. On the left, the green arrow suggests that the attraction of DPANN and Euryarchaeota by Bacteria could transform the correct 3D tree into the 2D tree on the right. On the right, the blue arrow suggests that the attraction of eukaryotes by Bacteria could transform the correct 2D tree into the 3D tree on the left.

Figure 4
Figure 4

RNA polymerase tree remains 3D after shortening the eukaryal branch. Maximum‐likelihood (ML) phylogenetic trees were constructed based on the concatenated two largest DNA‐dependent RNA polymerase subunits. ML phylogenetic trees are of the Bacteria, eukaryotes, and Archaea, including Asgard sequences from Lokiarchaeota (1 genome), Heimdallarchaeota (2 genomes), Odinarchaeota (1 genome), and Thorarchaeota (3 genomes). The tree on the left is from data set, while the tree on the right corresponds to the same data set and parameters but after the inclusion of sequences of the eukaryotic RNA polymerases I and III from data set. For consistency, the same method has been applied to both and is described in Da Cunha et al.. Briefly, the sequences were aligned with MAFFT v7 (default settings 29 ) and trimmed with BMGE (BLOSUM30 matrix 30 ). PhyML v3 was used for tree reconstruction with the BEST option for the tree search topology operations after the model was chosen according to the Akaike information criterion from ProtTest v3. The scale bars represent the average number of substitutions per site. Supports at branch correspond to nonparametric bootstrap (out of 100).

Figure 5
Figure 5

Explaining the patchy distribution of eukaryotic signature proteins (ESPs) in Asgards. Each color circle represents an ESP. Arrows with a similar color indicate their possible transfer from proto‐eukaryotes to Asgard at different periods of Asgard evolution. This is a schematic tree that emphasizes these specific transfers. The present patchy distribution of ESPs probably originated from a more complex pattern involving losses of ESPs in some archaeal lineages and horizontal gene transfer (HGT) between Asgard lineages. HGT of ESPs most likely also occurred between Asgard and other Archaea, as well as from Asgard to proto‐eukaryotes.

Figure 6
Figure 6

Phylogenetic trees of the universal protein Kae1/TsaD highlight the existence of different versions of Asgard proteins. From left to right. Initial 2D tree with DPANN at the base of Archaea and the fast‐evolving euryarchaeon Methanopyrus kandleri branching within paraphyletic Asgard (A), the 2D tree after removing fast‐evolving species (DPANN, M. kandleri) with Asgard divided into two monophyletic groups, one (two groups) sister group to Eukarya and the other (10 groups) branching between Euryarchaeota and the TACK clade (B) and the 3D tree obtained after further removing the two Asgard clades sister group to Eukarya (C). We observed in red several MAGs annotated as putative Bathyarchaota or Aigarchaeota that could be results of HGT or new groups of Asgard (C). The trimmed alignment provided of the Kae1/TsaD protein was selected from

https://doi.org/10.5281/zenodo.4624280

. The maximum likelihood trees were constructed using IQ‐TREE version 1.6.1239 under the model of evolution according to the MFP option for model selection. Values at nodes represent branch supports calculated with the Shimodaira–Hasegawa‐like approximate likelihood ratio test (aLRT) (10,000 replicates) and UFBoot (10,000 replicates), and a dot is indicated if the aLRT >80 or UFBoot >95. The scale bar represents the average number of substitutions per site. The trees will be available on figshare (

https://figshare.com/s/9e93072a77c3e014efd0

).

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