Abstract
The recently discovered DPANN archaea are a potentially deep-branching, monophyletic radiation of organisms with small cells and genomes. However, the monophyly and early emergence of the various DPANN clades and their role in life’s evolution are debated. Here, we reconstructed and analysed genomes of an uncharacterized archaeal phylum (Candidatus Undinarchaeota), revealing that its members have small genomes and, while potentially being able to conserve energy through fermentation, likely depend on partner organisms for the acquisition of certain metabolites. Our phylogenomic analyses robustly place Undinarchaeota as an independent lineage between two highly supported ‘DPANN’ clans. Further, our analyses suggest that DPANN have exchanged core genes with their hosts, adding to the difficulty of placing DPANN in the tree of life. This pattern can be sufficiently dominant to allow identifying known symbiont-host clades based on routes of gene transfer. Together, our work provides insights into the origins and evolution of DPANN and their hosts.
Highlights
The recently discovered DPANN archaea are a potentially deep-branching, monophyletic radiation of organisms with small cells and genomes
The generation of a large diversity of metagenomeassembled genomes (MAGs) representing archaeal and bacterial lineages across the tree of life has led to the definition of the tentative archaeal Uncultivated Archaeal Phylum 2 (UAP2) phylum[41]
The UAP2 MAGs have small genomes with an average size of 0.66 Mbp, coding for an average of 750 proteins. They likely represent a distinct archaeal phylum-level lineage based on average amino-acid identity (AAI) comparisons with other archaeal taxa (Supplementary Fig. 2, Supplementary Data 3), phylogenetic analyses including a concatenated 16S-23S rRNA gene tree (Supplementary Figs. 3–5 and see below) as well as classification based on the Genome Taxonomy Database (GTDB) rank normalization (Table 1, Supplementary Data 2)
Summary
The recently discovered DPANN archaea are a potentially deep-branching, monophyletic radiation of organisms with small cells and genomes. Analyses focusing on the placement of selected DPANN lineages in isolation, such as Nanoarchaeota and Parvarchaeota, relative to other Archaea, have led to the conclusion that these represent fast-evolving Euryarchaeota[28,29] It is debated whether the free-living Altiarchaeota belong to the DPANN radiation, form an independent lineage or belong to Euryarchaeota[8,10,13,30,31]. A potential cause for these conflicting topologies is that DPANN are often found on long branches in phylogenetic trees; these long branches might result from compositional biases or fast evolutionary rates[32,33] (as seen for obligate bacterial endosymbionts34,35) or might reflect genomic undersampling of the true diversity of this group[10] These alternatives are difficult to distinguish because, in the absence of fossils or definitive geochemical traces in the fossil record, we lack a well-constrained timescale for archaeal evolution. Ways to ameliorate such artefacts include increased taxonomic sampling[36], use of phylogenetic models less prone to LBA37, and the removal of fastevolving or compositionally biased sites from the alignment[38]
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