Horizontal gene transfer and gene loss drove the divergent evolution of host dependency in Micrarchaeota

Abstract The DPANN superphylum is a deep-branching radiation of Archaea with small cell and genome sizes. Most DPANN lineages are predicted or validated to be host-dependent. However, certain lineages have substantial biosynthetic capacities and are potentially less dependent on hosts or even free-living. Here, we reconstructed 163 Micrarchaeota genomes, comprising 48 assigned to previously undescribed orders and 115 affiliated with known orders. Investigation of their genetic repertoire revealed substantial metabolic capacity in Norongarragalinales, Anstonellales, and the newly proposed Wunengiarchaeales-associated lineages, including complete or near-complete glycolysis and de novo biosynthetic pathways for nucleotides, amino acids, co-factors, and cell envelopes. We classified these genes related to central metabolism, but which are uncommon in DPANN archaea as putative free-living associated genes (pFLAGs). The extensive presence of pFLAGs in Norongarragalinales suggests a potential host-independent lifestyle. Reconstruction of evolutionary history revealed that these pFLAGs were not ancestral within the DPANN superphylum. Instead, we suggest that less host-dependent organisms evolved from symbionts through the gradual acquisition of pFLAGs through horizontal gene transfer, whereas other Micrarchaeota lineages with streamlined genomes experienced reductive evolution due to thermal adaptation. Our analyses demonstrate that host dependency is not always an evolutionary dead end, but can be reversed through acquisition of new metabolic capabilities by horizontal transfer.