A phased chromosome-level genome of the annelid tubeworm Galeolaria caespitosa

Abstract

Haplotype-resolved (phased) genome assemblies are emerging as important assets for genomic studies of species with high heterozygosity, but remain lacking for key animal lineages. Here, we use PacBio HiFi and Omni-C technologies to assemble the first phased, annotated, chromosome-level genome for any annelid: the reef-building tubeworm Galeolaria caespitosa (Serpulidae). The assembly is 803.5 Mbp long (scaffold N50 = 76.5 Mbp) for haplotype 1 and 789.3 Mbp long (scaffold N50 = 75.4 Mbp) for haplotype 2, which are arranged into 11 pairs of chromosomes showing no sign of sex chromosomes. This compares with cytological analyses reporting 12 to 13 pairs in G. caespitosa's closest relatives, including species that are protandrous hermaphrodites. We combined long-read and short-read transcriptome sequencing to annotate both haplotypes, resulting in 30,495 predicted proteins for haplotype 1, 27,423 proteins for haplotype two, and 79.5% of proteins with at least one functional annotation. We also assembled a mitochondrial genome 23 kbp long, annotating all genes typically found in mitochondrial DNA apart from those coding the 16S ribosomal subunit (rrnL) and the protein atp8-a short, fast-evolving mitochondrial gene missing in other metazoans. Comparing G. caespitosa's genome to those of three other annelids reveals limited collinearity despite 36.0% of shared orthologous gene clusters (4,238 of 11,763 clusters counted in G. caespitosa), suggesting extensive chromosomal rearrangements among lineages. New high-quality annelid genomes may help resolve the genetic and evolutionary basis of this diversity.

Keywords: Annelida; Polychaeta; annotated reference genome; ecosystem engineer; marine invertebrate; mitochondria.

Fig. 1.

Circos plot of the 11 chromosomes in the phased assembly. From outside to inside: chromosomes of haplotype 1 (blue) and haplotype 2 (green), GC%, gene density (red), repeat density (blue), and Galeolaria  caespitosa adults retracted into tubes at low tide (photo credit: E. Chirgwin). GC%, gene density, and repeat density were estimated in 500 Kb windows with a 100 Kb step.

Fig. 2.

Comparative analyses of annelid genomes. (B) Counts of orthologous gene clusters shared between, Streblospio benedicti, Helobdella robusta, and Capitella teleta. (C) Collinearity analysis of Helobdella robusta, Streblospio benedicti, and Galeolaria caespitosa genomes. Note that no synteny was detected between genomes of H. robusta and S. benedicti. Genomes are labelled by chromosome number except in the case of H. robusta, which is labelled by scaffold.