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Description
All mouthless catenulid flatworms of the genus Paracatenula are in a symbiotic relationship with the chemosynthetic bacteria Candidatus Riegeria. This ancient symbiosis has been established more than 400 MYA, the endosymbionts are strictly transmitted vertically and, based on a single symbiont genome, the symbionts still harbour all genes essential for the complete nutrition of their animal host. To reconstruct the evolutionary dynamics of this ancient and stable relationship with very divergent ecophysiological parameters compared to long-term endosymbioses in insects, we sequenced the metagenomes of more than 23 species sampled in different parts of the world. We then used assembly-graph based analyses of the metagenomes to reconstruct complete symbiont genomes as well as host phylogenetic markers. Based on phylogenetic analyses at the gene and genomic level, and chromosome scale comparative methods we detect specific coevolutionary patterns for several host clades, and convergent patterns of streamlining and recombinatory stasis of the symbiont genome. The genome streamlining down to an average genome size of 1.36 Mb from roughly 5 Mb appears to precede the radiation of all extant Paracatenula species. Despite the age of the association, no essential functions show signs of decay, suggesting an immortalizing selection for genomic stability of the symbionts.