Genome and transcriptome mechanisms driving cephalopod evolution

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Albertin, C. B., Medina-Ruiz, S., Mitros, T., Schmidbaur, H., Sanchez, G., Wang, Z. Y., Grimwood, J., Rosenthal, J. J. C., Ragsdale, C. W., Simakov, O., & Rokhsar, D. S. Genome and transcriptome mechanisms driving cephalopod evolution. Nature Communications, 13(1), (2022): 2427, https://doi.org/10.1038/s41467-022-29748-w.Cephalopods are known for their large nervous systems, complex behaviors and morphological innovations. To investigate the genomic underpinnings of these features, we assembled the chromosomes of the Boston market squid, Doryteuthis (Loligo) pealeii, and the California two-spot octopus, Octopus bimaculoides, and compared them with those of the Hawaiian bobtail squid, Euprymna scolopes. The genomes of the soft-bodied (coleoid) cephalopods are highly rearranged relative to other extant molluscs, indicating an intense, early burst of genome restructuring. The coleoid genomes feature multi-megabase, tandem arrays of genes associated with brain development and cephalopod-specific innovations. We find that a known coleoid hallmark, extensive A-to-I mRNA editing, displays two fundamentally distinct patterns: one exclusive to the nervous system and concentrated in genic sequences, the other widespread and directed toward repetitive elements. We conclude that coleoid novelty is mediated in part by substantial genome reorganization, gene family expansion, and tissue-dependent mRNA editing.We thank the Marine Resources Center and the Cephalopod program at the Marine Biological Laboratory for supplying D. pealeii, R. Hanlon for the image in Fig. 1a, R. Hanlon and S. Senft for help with tissue dissection, Dr. Chuck Winkler for supplying O. bimaculoides, B. Burford and W. Gilly for assistance with D. opalescens collection, and the Vienna Zoo (Tiergarten Schönbrunn), particularly R. Halbauer, A. Weissenbacher, and the aquarist team for E. scolopes husbandry. Computation was done using the Life Science Cluster at the University of Vienna. This project began with generous funding from the Grass Foundation, administered by the MBL through J.J.R. It was also supported by Austrian Science fund FWF (P30686-B29) to H.S. and O.S., the Whitman Center Early Career Fellowship to O.S., the Okinawa Institute of Science and Technology Molecular Genetics Unit, Chan-Zuckerberg BioHub, and the Marthella Foskett Brown Chair in Computational Biology to D.S.R, NSF grant (IOS-1354898) to C.W.R, and the Hibbitt Early Career Fellowship to C.B.A. Sequencing at the University of Chicago Functional Genomics Facility was partially supported by the NIH (5UL1TR002389-02 and UL1 TR000430)