The Chromosome-level Genome of the Ctenophore Mnemiopsis leidyi A. Agassiz, 1865 Reveals a Unique Immune Gene Repertoire

18 pages, 5 figures, 1 table, supplementary material https://doi.org/10.1093/gbe/evaf006.-- Data Availability: Chromosome-level genome assembly of M. leidyi generated in this study is available at the European Nucleotide Archive (ENA) under the study ID PRJEB71361 and accession GCA_963919725

Ctenophora are basal marine metazoans, the sister group of all other animals. Mnemiopsis leidyi is one of the most successful invasive species worldwide with intense ecological and evolutionary research interest. Here, we generated a chromosome-level genome assembly of M. leidyi with a focus on its immune gene repertoire. The genome was 247.97 Mb, with N50 16.84 Mb, and 84.7% completeness. Its karyotype was 13 chromosomes. In this genome and that of two other ctenophores, Bolinopsis microptera and Hormiphora californensis, we detected a high number of protein domains related to potential immune receptors. Among those, proteins containing Toll/interleukin-1 (TIR2) domain, NACHT domain, Scavenger Receptor Cystein-Rich (SRCR) domain, or C-type Lectin domain (CTLD) were abundant and presented unique domain architectures in M. leidyi. M. leidyi seems to lack bona fide Toll-like Receptors, but it does possess a repertoire of 15 TIR2 domain-containing genes. Besides, we detected a bona fide NOD-like receptor and 38 NACHT domain-containing genes. In order to verify the function of those domain-containing genes, we exposed M. leidyi to the pathogen Vibrio coralliilyticus. Among the differentially expressed genes, we identified potential immune receptors, including four TIR2 domain-containing genes, all of which were upregulated in response to pathogen exposure. To conclude, many common immune receptor domains, highly conserved across metazoans, are already present in Ctenophora. These domains have large expansions and unique architectures in M. leidyi, findings consistent with the basal evolutionary position of this group, but still might have conserved functions in immunity and host–microbe interaction

This work was funded by the Deutsche Forschungsgemeinschaft (DFG) Sequencing Call proposal IMMUBASE [417981041 to L.P, R.S.S. and T.B.H.R]; and by the Collaborative Research Centre of Deutsche Forschungsgemeinschaft “Origin and Function of Metaorganisms (CRC1182)” (B2) [261376515 to R.S.S. and T.B.H.R]. Additional funding support was provided by “la Caixa” Foundation, Spain (to L.P.), [ID 10010434 to L.P.], co-financed by the European Union Horizon 2020 research and innovation program under the Marie Sklodowska-Curie Action grant agreement No 847648 [104855]; and by the “Severo-Ochoa Centre of Excellence” accreditation [CEX2019-000928-S]. This is a contribution from the Marine Biogeochemistry and Global Change research group Grant 2021SGR00430, Generalitat de Catalunya, Spain (to L.P.)

Peer reviewed