Annelid genomes: Enchytraeus crypticus, a soil model for the innate (and primed) immune system

Abstract

Enchytraeids (Annelida) are soil invertebrates with worldwide distribution that have served as ecotoxicology models for over 20 years. We present the first high-quality reference genome of Enchytraeus crypticus, assembled from a combination of Pacific Bioscience single-molecule real-time and Illumina sequencing platforms as a 525.2 Mbp genome (910 gapless scaffolds and 18,452 genes). We highlight isopenicillin, acquired by horizontal gene transfer and conferring antibiotic function. Significant gene family expansions associated with regeneration (long interspersed nuclear elements), the innate immune system (tripartite motif-containing protein) and response to stress (cytochrome P450) were identified. The ACE (Angiotensin-converting enzyme) - a homolog of ACE2, which is involved in the coronavirus SARS-CoV-2 cell entry - is also present in E. crypticus. There is an obvious potential of using E. crypticus as a model to study interactions between regeneration, the innate immune system and aging-dependent decline.

Fig. 1. Enchytraeus crypticus (Annelida: Enchytraeidae).

E. crypticus are soil invertebrates, belonging to the Oligochaete. Their size ranges from 6 to 9 mm, and they reproduce both sexually and asexually, carrying the cocoons with the embryos in the clitellum and releasing these when matured; they are semi-transparent, and the cocoons and other organelles can be visualized directly (e.g., under a binocular in the culture dishes). a, A photo in a natural habitat assembly. b, A cocoon with embryos. c, A cocoon at post-eggs stage (start of differentiation). d, A cocoon with juveniles. e, Juveniles from a hatched cocoon; f, An adult.

Fig. 2. Enchytraeus crypticus genome.

a, GO (Gene Ontology) functional distribution, including the top 50 per biological process, molecular function and cellular component. b, Ultrametric phylogenetic tree based on orthogroup analysis from this study. The indicative age of the root was derived from the TimeTree database divergence time of C. elegans to all members of the clade composed by F. candida, D. pulex and D. melanogaster. c, Comparative analysis via Venn diagram, displaying the number of shared gene families between Annelids (E. crypticus, E. fetida, E. andrei, H. robusta and C. teleta) as determined by OrthoFinder.

Fig. 3. Synteny plot showing intra- and inter-scaffold collinear genes in the E. crypticus genome.

Scaffolds were renumbered after ordering them by decreasing length for readability; only relevant scaffolds are shown. Gray bars represent scaffolds with no collinearity in the context shown. Scale in million bp. a, Inter-scaffold collinearity. b, Intra-scaffold collinearity; palindromes are drawn with blue links, tandem repeats with red links.

Fig. 4. Horizontally transferred genes (HTG) in Enchytraeus crypticus.

a, Origin. b, Enriched Gene Ontology. Supplementary Table 11 contains the P values for the GO terms.