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  • 1
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    A draft genome sequence of the elusive giant squid, Architeuthis dux (2020)
    Oxford University Press
    Details
    Publication Date: 2023-02-08
    Description: Background: The giant squid (Architeuthis dux; Steenstrup, 1857) is an enigmatic giant mollusc with a circumglobal distribution in the deep ocean, except in the high Arctic and Antarctic waters. The elusiveness of the species makes it difficult to study. Thus, having a genome assembled for this deep-sea-dwelling species will allow several pending evolutionary questions to be unlocked. Findings: We present a draft genome assembly that includes 200 Gb of Illumina reads, 4 Gb of Moleculo synthetic long reads, and 108 Gb of Chicago libraries, with a final size matching the estimated genome size of 2.7 Gb, and a scaffold N50 of 4.8 Mb. We also present an alternative assembly including 27 Gb raw reads generated using the Pacific Biosciences platform. In addition, we sequenced the proteome of the same individual and RNA from 3 different tissue types from 3 other species of squid (Onychoteuthis banksii, Dosidicus gigas, and Sthenoteuthis oualaniensis) to assist genome annotation. We annotated 33,406 protein-coding genes supported by evidence, and the genome completeness estimated by BUSCO reached 92%. Repetitive regions cover 49.17% of the genome. Conclusions: This annotated draft genome of A. dux provides a critical resource to investigate the unique traits of this species, including its gigantism and key adaptations to deep-sea environments.
    Type: Article , PeerReviewed
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  • 2
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    A draft genome sequence of the elusive giant squid, Architeuthis dux (2020)
    Oxford University Press
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in da Fonseca, R. R., Couto, A., Machado, A. M., Brejova, B., Albertin, C. B., Silva, F., Gardner, P., Baril, T., Hayward, A., Campos, A., Ribeiro, A. M., Barrio-Hernandez, I., Hoving, H. J., Tafur-Jimenez, R., Chu, C., Frazao, B., Petersen, B., Penaloza, F., Musacchia, F., Alexander, G. C., Osorio, H., Winkelmann, I., Simakov, O., Rasmussen, S., Rahman, M. Z., Pisani, D., Vinther, J., Jarvis, E., Zhang, G., Strugnell, J. M., Castro, L. F. C., Fedrigo, O., Patricio, M., Li, Q., Rocha, S., Antunes, A., Wu, Y., Ma, B., Sanges, R., Vinar, T., Blagoev, B., Sicheritz-Ponten, T., Nielsen, R., & Gilbert, M. T. P. A draft genome sequence of the elusive giant squid, Architeuthis dux. Gigascience, 9(1), (2020): giz152. doi: 10.1093/gigascience/giz152.
    Description: Background: The giant squid (Architeuthis dux; Steenstrup, 1857) is an enigmatic giant mollusc with a circumglobal distribution in the deep ocean, except in the high Arctic and Antarctic waters. The elusiveness of the species makes it difficult to study. Thus, having a genome assembled for this deep-sea–dwelling species will allow several pending evolutionary questions to be unlocked. Findings: We present a draft genome assembly that includes 200 Gb of Illumina reads, 4 Gb of Moleculo synthetic long reads, and 108 Gb of Chicago libraries, with a final size matching the estimated genome size of 2.7 Gb, and a scaffold N50 of 4.8 Mb. We also present an alternative assembly including 27 Gb raw reads generated using the Pacific Biosciences platform. In addition, we sequenced the proteome of the same individual and RNA from 3 different tissue types from 3 other species of squid (Onychoteuthis banksii, Dosidicus gigas, and Sthenoteuthis oualaniensis) to assist genome annotation. We annotated 33,406 protein-coding genes supported by evidence, and the genome completeness estimated by BUSCO reached 92%. Repetitive regions cover 49.17% of the genome. Conclusions: This annotated draft genome of A. dux provides a critical resource to investigate the unique traits of this species, including its gigantism and key adaptations to deep-sea environments.
    Description: R.R.F. thanks the Villum Fonden for grant VKR023446 (Villum Fonden Young Investigator Grant), the Portuguese Science Foundation (FCT) for grant PTDC/MAR/115347/2009; COMPETE-FCOMP-01-012; FEDER-015453, Marie Curie Actions (FP7-PEOPLE-2010-IEF, Proposal 272927), and the Danish National Research Foundation (DNRF96) for its funding of the Center for Macroecology, Evolution, and Climate. H.O. thanks the Rede Nacional de Espectrometria de Massa, ROTEIRO/0028/2013, ref. LISBOA-01-0145-FEDER-022125, supported by COMPETE and North Portugal Regional Operational Programme (Norte2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). A.C. thanks FCT for project UID/Multi/04423/2019. M.P. acknowledges the support from the Wellcome Trust (grant number WT108749/Z/15/Z) and the European Molecular Biology Laboratory. M.P.T.G. thanks the Danish National Research Foundation for its funding of the Center for GeoGenetics (grant DNRF94) and Lundbeck Foundation for grant R52–5062 on Pathogen Palaeogenomics. S.R. was supported by the Novo Nordisk Foundation grant NNF14CC0001. A.H. is supported by a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (fellowship reference: BB/N020146/1). T.B. is supported by the Biotechnology and Biological Sciences Research Council-funded South West Biosciences Doctoral Training Partnership (training grant reference BB/M009122/1). This work was partially funded by the Lundbeck Foundation (R52-A4895 to B.B.). H.J.T.H. was supported by the David and Lucile Packard Foundation, the Netherlands Organization for Scientific Research (#825.09.016), and currently by the Deutsche Forschungsgemeinschaft (DFG) under grant HO 5569/2-1 (Emmy Noether Junior Research Group). T.V. and B. Brejova were supported by grants from the Slovak grant agency VEGA (1/0684/16, 1/0458/18). F.S. was supported by a PhD grant (SFRH/BD/126560/2016) from FCT. A.A. was partly supported by the FCT project PTDC/CTA-AMB/31774/2017. C.C. and Y.W. are partly supported by grant IIS-1526415 from the US National Science Foundation. Computation for the work described in this article was partially supported by the DeiC National Life Science Supercomputer at DTU.
    Keywords: Cephalopod ; Invertebrate ; Genome assembly
    Repository Name: Woods Hole Open Access Server
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  • 3
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    Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization (2022)
    Nature Research
    Details
    Publication Date: 2022-08-03
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Schmidbaur, H., Kawaguchi, A., Clarence, T., Fu, X., Hoang, O. P., Zimmermann, B., Ritschard, E. A., Weissenbacher, A., Foster, J. S., Nyholm, S., Bates, P. A., Albertin, C. B., Tanaka, E., & Simakov, O. Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization. Nature Communications, 13(1), (2022): 2172, https://doi.org/10.1038/s41467-022-29694-7.
    Description: Coleoid cephalopods (squid, cuttlefish, octopus) have the largest nervous system among invertebrates that together with many lineage-specific morphological traits enables complex behaviors. The genomic basis underlying these innovations remains unknown. Using comparative and functional genomics in the model squid Euprymna scolopes, we reveal the unique genomic, topological, and regulatory organization of cephalopod genomes. We show that coleoid cephalopod genomes have been extensively restructured compared to other animals, leading to the emergence of hundreds of tightly linked and evolutionary unique gene clusters (microsyntenies). Such novel microsyntenies correspond to topological compartments with a distinct regulatory structure and contribute to complex expression patterns. In particular, we identify a set of microsyntenies associated with cephalopod innovations (MACIs) broadly enriched in cephalopod nervous system expression. We posit that the emergence of MACIs was instrumental to cephalopod nervous system evolution and propose that microsyntenic profiling will be central to understanding cephalopod innovations.
    Description: H.S., O.P.H., E.R., and O.S. were supported by the Austrian Science Fund (FWF) grant P30686-B29. O.S. was supported by Whitman Center Early Career Fellowship (Frank R. Lillie Quasi-Endowment Fund, L. & A. Colwin Summer Research Fellowship, Bell Research Award in Tissue Engineering). H.S. was supported by the short-term grant abroad (KWA) of the University of Vienna. H.S. and O.S. were supported by the University of Chicago/Vienna Strategic Partnership Programme Mobility Grant. A.K. was supported by the JSPS Postdoctoral Fellowship for Overseas Researchers program from Japan. C.B.A. was supported by the Hibbitt Early Career Fellowship. Eggs and paralarvae of E. scolopes were generated in part by support by the NASA Space Biology 80NSSC18K1465 awarded to J.S.F. S.V.N. was supported by the National Science Foundation IOS-1557914. This work was supported by the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC0001003), the UK Medical Research Council (FC001003), and the Wellcome Trust (FC001003).
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  • 4
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    Genome and transcriptome mechanisms driving cephalopod evolution (2022)
    Nature Research
    Details
    Publication Date: 2022-08-19
    Description: © 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.
    Description: 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.
    Description: 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).
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  • 5
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    Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain (2022)
    BMC
    Details
    Publication Date: 2022-09-01
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Petrosino, G., Ponte, G., Volpe, M., Zarrella, I., Ansaloni, F., Langella, C., Di Cristina, G., Finaurini, S., Russo, M., Basu, S., Musacchia, F., Ristoratore, F., Pavlinic, D., Benes, V., Ferrante, M., Albertin, C., Simakov, O., Gustincich, S., Fiorito, G., & Sanges, R. Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain. BMC Biology, 20(1) (2022): 116, https://doi.org/10.1186/s12915-022-01303-5.
    Description: Background Transposable elements (TEs) widely contribute to the evolution of genomes allowing genomic innovations, generating germinal and somatic heterogeneity, and giving birth to long non-coding RNAs (lncRNAs). These features have been associated to the evolution, functioning, and complexity of the nervous system at such a level that somatic retrotransposition of long interspersed element (LINE) L1 has been proposed to be associated to human cognition. Among invertebrates, octopuses are fascinating animals whose nervous system reaches a high level of complexity achieving sophisticated cognitive abilities. The sequencing of the genome of the Octopus bimaculoides revealed a striking expansion of TEs which were proposed to have contributed to the evolution of its complex nervous system. We recently found a similar expansion also in the genome of Octopus vulgaris. However, a specific search for the existence and the transcription of full-length transpositionally competent TEs has not been performed in this genus. Results Here, we report the identification of LINE elements competent for retrotransposition in Octopus vulgaris and Octopus bimaculoides and show evidence suggesting that they might be transcribed and determine germline and somatic polymorphisms especially in the brain. Transcription and translation measured for one of these elements resulted in specific signals in neurons belonging to areas associated with behavioral plasticity. We also report the transcription of thousands of lncRNAs and the pervasive inclusion of TE fragments in the transcriptomes of both Octopus species, further testifying the crucial activity of TEs in the evolution of the octopus genomes. Conclusions The neural transcriptome of the octopus shows the transcription of thousands of putative lncRNAs and of a full-length LINE element belonging to the RTE class. We speculate that a convergent evolutionary process involving retrotransposons activity in the brain has been important for the evolution of sophisticated cognitive abilities in this genus.
    Description: The work has been supported by Progetto Premiale MolEcOC (Italian Ministry of Education, University and Research, MIUR), Flagship project RITMARE (MIUR and Stazione Zoologica), and BIOforIU PON Project (MIUR and European Regional Development Fund, FESR). Giuseppe Petrosino, Swaraj Basu, Massimiliano Volpe, and Giulia Di Cristina have been supported by a SZN PhD fellowship.
    Keywords: Mollusks ; Nervous system ; Transcriptome ; Transposable elements
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  • 6
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    The evolution of synaptic and cognitive capacity: insights from the nervous system transcriptome of Aplysia (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-11-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Orvis, J., Albertin, C., Shrestha, P., Chen, S., Zheng, M., Rodriguez, C., Tallon, L., Mahurkar, A., Zimin, A., Kim, M., Liu, K., Kandel, E., Fraser, C., Sossin, W., & Abrams, T. The evolution of synaptic and cognitive capacity: insights from the nervous system transcriptome of Aplysia. Proceedings of the National Academy of Sciences of the United States of America, 119(28), (2022): e2122301119, https://doi.org/10.1073/pnas.2122301119.
    Description: The gastropod mollusk Aplysia is an important model for cellular and molecular neurobiological studies, particularly for investigations of molecular mechanisms of learning and memory. We developed an optimized assembly pipeline to generate an improved Aplysia nervous system transcriptome. This improved transcriptome enabled us to explore the evolution of cognitive capacity at the molecular level. Were there evolutionary expansions of neuronal genes between this relatively simple gastropod Aplysia (20,000 neurons) and Octopus (500 million neurons), the invertebrate with the most elaborate neuronal circuitry and greatest behavioral complexity? Are the tremendous advances in cognitive power in vertebrates explained by expansion of the synaptic proteome that resulted from multiple rounds of whole genome duplication in this clade? Overall, the complement of genes linked to neuronal function is similar between Octopus and Aplysia. As expected, a number of synaptic scaffold proteins have more isoforms in humans than in Aplysia or Octopus. However, several scaffold families present in mollusks and other protostomes are absent in vertebrates, including the Fifes, Lev10s, SOLs, and a NETO family. Thus, whereas vertebrates have more scaffold isoforms from select families, invertebrates have additional scaffold protein families not found in vertebrates. This analysis provides insights into the evolution of the synaptic proteome. Both synaptic proteins and synaptic plasticity evolved gradually, yet the last deuterostome-protostome common ancestor already possessed an elaborate suite of genes associated with synaptic function, and critical for synaptic plasticity.
    Description: This work was supported by NSF EAGER Award IOS-1255695 and NIH grant R01 MH 55880 grant to T.W.A.; by a Natural Sciences and Engineering Research Council of Canada Discovery grant and Canadian Institutes of Health Research project grant 340328 to W.S.; by funding from the HHMI to E.R.K.; and by a Hibbitt Early Career Fellowship to C.A. W.S. is James McGill Professor at McGill University.
    Keywords: Neural plasticity ; Synaptic plasticity ; Evolution ; Neuromodulation ; Aplysia
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