Simakov Oleg

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  • Article
    Genome and transcriptome mechanisms driving cephalopod evolution
    (Nature Research, 2022-05-04) Albertin, Carolin B. ; Medina-Ruiz, Sofia ; Mitros, Therese ; Schmidbaur, Hannah ; Sanchez, Gustavo ; Wang, Z. Yan ; Grimwood, Jane ; Rosenthal, Joshua J. C. ; Ragsdale, Clifton W. ; Simakov, Oleg ; Rokhsar, Daniel S.
    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.
  • Article
    A draft genome sequence of the elusive giant squid, Architeuthis dux
    (Oxford University Press, 2020-01-16) da Fonseca, Rute R. ; Couto, Alvarina ; Machado, Andre M. ; Brejova, Brona ; Albertin, Carolin B. ; Silva, Filipe ; Gardner, Paul ; Baril, Tobias ; Hayward, Alex ; Campos, Alexandre ; Ribeiro, Ângela M. ; Barrio-Hernandez, Inigo ; Hoving, Henk-Jan ; Tafur-Jimenez, Ricardo ; Chu, Chong ; Frazão, Barbara ; Petersen, Bent ; Peñaloza, Fernando ; Musacchia, Francesco ; Alexander, Graham C., Jr. ; Osório, Hugo ; Winkelmann, Inger ; Simakov, Oleg ; Rasmussen, Simon ; Rahman, M. Ziaur ; Pisani, Davide ; Vinther, Jakob ; Jarvis, Erich ; Zhang, Guojie ; Strugnell, Jan M. ; Castro, L. Filipe C. ; Fedrigo, Olivier ; Patricio, Mateus ; Li, Qiye ; Rocha, Sara ; Antunes, Agostinho ; Wu, Yufeng ; Ma, Bin ; Sanges, Remo ; Vinar, Tomas ; Blagoev, Blagoy ; Sicheritz-Ponten, Thomas ; Nielsen, Rasmus ; Gilbert, M. Thomas P.
    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.
  • Article
    Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
    (BMC, 2022-05-18) Petrosino, Giuseppe ; Ponte, Giovanna ; Volpe, Massimiliano ; Zarrella, Ilaria ; Ansaloni, Federico ; Langella, Concetta ; Di Cristina, Giulia ; Finaurini, Sara ; Russo, Monia T. ; Basu, Swaraj ; Musacchia, Francesco ; Ristoratore, Filomena ; Pavlinic, Dinko ; Benes, Vladimir ; Ferrante, Maria I. ; Albertin, Carolin B. ; Simakov, Oleg ; Gustincich, Stefano ; Sanges, Remo
    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.
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    Bilaterian phylogenetic trees
    ( 2014-12-19) Albertin, Caroline B. ; Simakov, Oleg ; Mitros, Therese ; Wang, Z. Yan ; Pungor, Judit R. ; Edsinger-Gonzales, Eric ; Brenner, Sydney ; Ragsdale, Clifton W. ; Rokhsar, Daniel S
  • Article
    Coupled genomic evolutionary histories as signatures of organismal innovations in cephalopods: co-evolutionary signatures across levels of genome organization may shed light on functional linkage and origin of cephalopod novelties
    (Wiley, 2019-10-30) Ritschard, Elena A. ; Whitelaw, Brooke ; Albertin, Caroline B. ; Cooke, Ira R. ; Strugnell, Jan M. ; Simakov, Oleg
    How genomic innovation translates into organismal organization remains largely unanswered. Possessing the largest invertebrate nervous system, in conjunction with many species‐specific organs, coleoid cephalopods (octopuses, squids, cuttlefishes) provide exciting model systems to investigate how organismal novelties evolve. However, dissecting these processes requires novel approaches that enable deeper interrogation of genome evolution. Here, the existence of specific sets of genomic co‐evolutionary signatures between expanded gene families, genome reorganization, and novel genes is posited. It is reasoned that their co‐evolution has contributed to the complex organization of cephalopod nervous systems and the emergence of ecologically unique organs. In the course of reviewing this field, how the first cephalopod genomic studies have begun to shed light on the molecular underpinnings of morphological novelty is illustrated and their impact on directing future research is described. It is argued that the application and evolutionary profiling of evolutionary signatures from these studies will help identify and dissect the organismal principles of cephalopod innovations. By providing specific examples, the implications of this approach both within and beyond cephalopod biology are discussed.
  • Article
    Emergence of novel cephalopod gene regulation and expression through large-scale genome reorganization
    (Nature Research, 2022-04-21) Schmidbaur, Hannah ; Kawaguchi, Akane ; Clarence, Tereza ; Fu, Xiao ; Hoang, Oi Pui ; Zimmermann, Bob ; Ritschard, Elena A. ; Weissenbacher, Anton ; Foster, Jamie S. ; Nyholm, Spencer V. ; Bates, Paul A. ; Albertin, Carolin B. ; Tanaka, Elly ; Simakov, Oleg
    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.
  • Article
    The African coelacanth genome provides insights into tetrapod evolution
    (Nature Publishing Group, 2013-04-17) Amemiya, Chris T. ; Alfoldi, Jessica ; Lee, Alison P. ; Fan, Shaohua ; Philippe, Herve ; MacCallum, Iain ; Braasch, Ingo ; Manousaki, Tereza ; Schneider, Igor ; Rohner, Nicolas ; Organ, Chris ; Chalopin, Domitille ; Smith, Jeramiah J. ; Robinson, Mark ; Dorrington, Rosemary A. ; Gerdol, Marco ; Aken, Bronwen ; Assunta Biscotti, Maria ; Barucca, Marco ; Baurain, Denis ; Berlin, Aaron M. ; Blatch, Gregory L. ; Buonocore, Francesco ; Burmester, Thorsten ; Campbell, Michael S. ; Canapa, Adriana ; Cannon, John P. ; Christoffels, Alan ; De Moro, Gianluca ; Edkins, Adrienne L. ; Fan, Lin ; Fausto, Anna Maria ; Feiner, Nathalie ; Forconi, Mariko ; Gamieldien, Junaid ; Gnerre, Sante ; Gnirke, Andreas ; Goldstone, Jared V. ; Haerty, Wilfried ; Hahn, Mark E. ; Hesse, Uljana ; Hoffmann, Steve ; Johnson, Jeremy ; Karchner, Sibel I. ; Kuraku, Shigehiro ; Lara, Marcia ; Levin, Joshua Z. ; Litman, Gary W. ; Mauceli, Evan ; Miyake, Tsutomu ; Mueller, M. Gail ; Nelson, David R. ; Nitsche, Anne ; Olmo, Ettore ; Ota, Tatsuya ; Pallavicini, Alberto ; Panji, Sumir ; Picone, Barbara ; Ponting, Chris P. ; Prohaska, Sonja J. ; Przybylski, Dariusz ; Ratan Saha, Nil ; Ravi, Vydianathan ; Ribeiro, Filipe J. ; Sauka-Spengler, Tatjana ; Scapigliati, Giuseppe ; Searle, Stephen M. J. ; Sharpe, Ted ; Simakov, Oleg ; Stadler, Peter F. ; Stegeman, John J. ; Sumiyama, Kenta ; Tabbaa, Diana ; Tafer, Hakim ; Turner-Maier, Jason ; van Heusden, Peter ; White, Simon ; Williams, Louise ; Yandell, Mark ; Brinkmann, Henner ; Volff, Jean-Nicolas ; Tabin, Clifford J. ; Shubin, Neil ; Schartl, Manfred ; Jaffe, David B. ; Postlethwait, John H. ; Venkatesh, Byrappa ; Di Palma, Federica ; Lander, Eric S. ; Meyer, Axel ; Lindblad-Toh, Kerstin
    The discovery of a living coelacanth specimen in 1938 was remarkable, as this lineage of lobe-finned fish was thought to have become extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features. Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues show the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.
  • Article
    The Nereid on the rise: Platynereis as a model system
    (BMC, 2021-09-27) Ozpolat, B. Duygu ; Randel, Nadine ; Williams, Elizabeth A. ; Bezares-Calderón, Luis Alberto ; Andreatta, Gabriele ; Balavoine, Guillaume ; Bertucci, Paola Y. ; Ferrier, David E. K. ; Gambi, Maria Cristina ; Gazave, Eve ; Handberg-Thorsager, Mette ; Hardege, Jörg ; Hird, Cameron ; Hsieh, Yu-Wen ; Hui, Jerome ; Mutemi, Kevin Nzumbi ; Schneider, Stephan Q. ; Simakov, Oleg ; Vergara, Hernando M. ; Vervoort, Michel ; Jékely, Gáspár ; Tessmar-Raible, Kristin ; Raible, Florian ; Arendt, Detlev
    The Nereid Platynereis dumerilii (Audouin and Milne Edwards (Annales des Sciences Naturelles 1:195–269, 1833) is a marine annelid that belongs to the Nereididae, a family of errant polychaete worms. The Nereid shows a pelago-benthic life cycle: as a general characteristic for the superphylum of Lophotrochozoa/Spiralia, it has spirally cleaving embryos developing into swimming trochophore larvae. The larvae then metamorphose into benthic worms living in self-spun tubes on macroalgae. Platynereis is used as a model for genetics, regeneration, reproduction biology, development, evolution, chronobiology, neurobiology, ecology, ecotoxicology, and most recently also for connectomics and single-cell genomics. Research on the Nereid started with studies on eye development and spiralian embryogenesis in the nineteenth and early twentieth centuries. Transitioning into the molecular era, Platynereis research focused on posterior growth and regeneration, neuroendocrinology, circadian and lunar cycles, fertilization, and oocyte maturation. Other work covered segmentation, photoreceptors and other sensory cells, nephridia, and population dynamics. Most recently, the unique advantages of the Nereid young worm for whole-body volume electron microscopy and single-cell sequencing became apparent, enabling the tracing of all neurons in its rope-ladder-like central nervous system, and the construction of multimodal cellular atlases. Here, we provide an overview of current topics and methodologies for P. dumerilii, with the aim of stimulating further interest into our unique model and expanding the active and vibrant Platynereis community.