Distinct genomic adaptations of the methanogenic archaeal genus Methanocorpusculum to symbiosis with animals and protists

Most of our understanding of endosymbiosis originates from the bacterial endosymbionts of multicellular, terrestrial hosts, which represent habitats with dramatically different selective pressures than inside a protist cell. Methanogenic archaea from the genus Methanocorpusculum are among the few known intracellular archaea and form unique symbioses with both animal and protist hosts, providing a unique opportunity to contrast symbiont evolution and function in very distinct host types. Here, we conducted phylo- and pangenomic analyses on 106 Methanocorpusculum strains originating from animal and ciliate hosts as well as environmental habitats. We recovered two divergent clades corresponding to animal gut-associated and intracellular ciliate-associated/environmental lineages and found that ciliate-associated and environmental Methanocorpusculum are virtually indistinguishable functionally and phylogenetically. Ciliate-associated symbionts retained broad biosynthetic capacity and encoded functions related to osmotic stress tolerance and adhesion within the host cell, while animal gut-associated symbionts exhibited patterns of genome streamlining and nutrient scavenging consistent with host supply and immune adaptation. Our findings illuminate how the contrasting selective pressures of protists and animal hosts have driven divergent evolutionary and functional strategies in congeneric archaeal symbionts.