Undinarchaeota illuminate DPANN phylogeny and the impact of gene transfer on archaeal evolution

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.

Protein family content uncovers lineage relationships and bacterial pathway maintenance mechanisms in DPANN archaea

“…Similar patterns of gene loss on the path to symbioses could have arisen via convergent evolution or could indicate that phylogenetically distinct lineages have shared ancestry. Our findings related to lateral gene transfer extend those of a very recent report that suggested the phylogenetic analyses of DPANN archaea may be confounded by this process (Dombrowski et al, 2020) .…”

“…Halophilic nanoarchaea were found in archaea-dominated planktonic communities (Narasingarao et al, 2012) . Over time, a series of papers investigating the microbiology of sediments and aquatic environments greatly expanded the taxonomic diversity of nanoarchaea (Rinke et al, 2013a;Castelle et al, 2015a;Dombrowski et al, 2020) . One group, groundwater-associated Huberarchaeota, are predicted to be symbionts of the archaeal Altiarchaeota (SM1) based on highly correlated abundance patterns (Probst et al, 2018) .…”

Insights into synthesis and function of KsgA/Dim1-dependent rRNA modifications in archaea

“…Another peculiar aspect is the presence of type III h45 in the recently described Methanonatroarchaea and its absence in Nanohaloarchaeota. Noteworthy, the relative positioning of these organisms is disputed ( 112 , 135–137 ). Whereas our observations are still limited in their scope and depth to validate or invalidate phylogenetic relationship directly, our improved knowledge of ribosome biogenesis diversity in archaea will additionally contribute to refining evolutionary scenarios and phylogenetic relationship, in the form of ‘functional phylogenetic’.…”

Physical connections: prokaryotes parasitizing their kin

“…However, the monophyly and the basal placement of some DPANN lineages remain debated, notably of Nanoarchaeota and Nanohaloarchaeota, potentially related to Thermococcales and haloarchaea or other Euryarchaeota respectively (Brochier et al ., 2005; Petitjean et al ., 2014; Williams et al ., 2017; Aouad et al ., 2018). DPANN refers to the first named lineages of this group (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota) but it now encompasses over 10 phylum‐level clades (reviewed in Castelle and Banfield, 2018; Castelle et al ., 2018; Dombrowski et al ., 2019), including Diapherotrites, Altiarchaeota and Micrarchaeota, which cluster together, and Nanoarchaeota, Parvarchaeota, Pacearchaeota, Woesearchaeota, Huberarchaeota, Nanohaloarchaeota, Aenigmarchaeota and the recently identified Undinarchaeota (Dombrowski et al ., 2020). The vast majority of these organisms were identified from single‐cell genomes (SAGs) or metagenome‐assembled genomes (MAGs) and remain uncultured.…”