Phylogenomic analyses reveal that Panguiarchaeum is a clade of genome-reduced Asgard archaea

Abstract

The Asgard archaea are a diverse archaeal phylum important for our understanding of cellular evolution because they include the lineage that gave rise to eukaryotes. Recent phylogenomic work has focused on characterising the diversity of Asgard archaea in an effort to identify the closest extant relatives of eukaryotes. However, resolving archaeal phylogeny is challenging, and the positions of two recently-described lineages - Njordarchaeales and Panguiarchaeales - are uncertain, in ways that directly bear on hypotheses of early evolution. In initial phylogenetic analyses, these lineages branched either with Asgards or with the distantly-related Korarchaeota, and it has been suggested that their genomes may be affected by metagenomic contamination. Resolving this debate is important because these clades include genome-reduced lineages that may help inform our understanding of the evolution of symbiosis within Asgard archaea. Here, we performed phylogenetic analyses revealing that the Njordarchaeales and Pangiuarchaeales constitute the new class Njordarchaeia within Asgard archaea. We found no evidence of metagenomic contamination affecting phylogenetic analyses. Njordarchaeia exhibit hallmarks of adaptations to (hyper-)thermophilic lifestyles, including biased sequence compositions that can induce phylogenetic artifacts unless adequately modelled. Panguiarchaeum is metabolically distinct from its relatives, with reduced metabolic potential and various auxotrophies. Phylogenetic reconciliation recovers a complex common ancestor of Asgard archaea that encoded the Wood-Ljungdahl pathway. The subsequent loss of this pathway during the reductive evolution of Panguiarchaeum may have been associated with the switch to a symbiotic lifestyle based on H2-syntrophy. Thus, Panguiarchaeum may contain the first obligate symbionts within Asgard archaea.