Sea anemone genomes reveal ancestral metazoan chromosomal macrosynteny

Abstract

Draft genome sequences of non-bilaterian species have provided important insights into the evolution of the metazoan gene repertoire. However, there is little information about the evolution of gene clusters, genome architectures and karyotypes during animal evolution. In this regard, slowly evolving anthozoan Cnidaria, the sister group of Bilateria, are particularly informative. Here we report chromosome-level genome assemblies of two related cnidarians, the sea anemones Nematostella vectensis and Scolanthus callimorphus. We find a robust set of 15 chromosomes with a clear one-to-one correspondence between the two species. Both sea anemone genomes show remarkable chromosomal conservation with other cnidarians, several bilaterians and the sponge Ephydatia muelleri, allowing us to reconstruct ancestral cnidarian and metazoan chromosomal blocks, consisting of at least 19 and 16 ancestral linkage groups, respectively. We show that, in contrast to Bilateria, the Hox and NK clusters of investigated cnidarians are largely disintegrated, despite the presence of staggered hox/gbx expression in Nematostella. This loss of microsynteny conservation may be facilitated by shorter distances between cis-regulatory sequences and their cognate transcriptional start sites. In line with that, we find no clear evidence for topologically associated domains, suggesting fundamental differences in long-range gene regulation compared to vertebrates. These data suggest that large sets of ancestral metazoan genes have been retained in ancestral linkage groups of some extant lineages, yet, higher order gene regulation with associated 3D architecture may have evolved only after the cnidarian-bilaterian split.