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Alatina Alata (Cubozoa), Calvadosia Cruxmelitensis (Staurozoa), and Cassiopea Xamachana (Scyphozoa) Aki Ohdera 1, Cheryl L

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Alatina Alata (Cubozoa), Calvadosia Cruxmelitensis (Staurozoa), and Cassiopea Xamachana (Scyphozoa) Aki Ohdera 1, Cheryl L GigaScience, 8, 2019, 1–15 doi: 10.1093/gigascience/giz069 Data Note DATA NOTE Downloaded from https://academic.oup.com/gigascience/article-abstract/8/7/giz069/5524763 by guest on 03 July 2019 Box, stalked, and upside-down? Draft genomes from diverse jellyfish (Cnidaria, Acraspeda) lineages: Alatina alata (Cubozoa), Calvadosia cruxmelitensis (Staurozoa), and Cassiopea xamachana (Scyphozoa) Aki Ohdera 1, Cheryl L. Ames2,3, Rebecca B. Dikow4, Ehsan Kayal2,5, Marta Chiodin6,7, Ben Busby3, Sean La3,8,StacyPirro9, Allen G. Collins2,10, Monica´ Medina 1,* and Joseph F. Ryan 6,7,* 1Department of Biology, Pennsylvania State University, 326 Mueller, University Park, PA, 16801, USA; 2Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 10th Street & Constitution Avenue NW, Washington DC, 20560, USA; 3National Center for Biotechnology Information, 8600 Rockville Pike MSC 3830, Bethesda, MD, 20894, USA; 4Data Science Lab, Office of the Chief Information Officer, Smithsonian Institution, 10th Street & Constitution Avenue NW, Washington DC,20560, USA; 5UPMC, CNRS, FR2424, ABiMS, Station Biologique, Place Georges Teissier, 29680 Roscoff, France; 6Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Boulevard, St. Augustine, FL, 32080, USA; 7Department of Biology, University of Florida, 220 Bartram Hall, Gainesville, FL, 32611, USA; 8Department of Mathematics, Simon Fraser University, 8888 University Drive, Barnaby, British Columbia, BC, V5A 1S6, Canada; 9Iridian Genomes, Inc., 6213 Swords Way, Bethesda, MD, 20817, USA and 10National Systematics Laboratory of NOAA’s Fisheries Service, 1315 East-West Highway, Silver Spring, MD, 20910, USA ∗Correspondence address. Joseph F. Ryan, Address: 9505 Ocean Shore Boulevard, St. Augustine, FL, 32080, USA; E-mail: [email protected] http://orcid.org/0000-0001-8367-0293;. Monica´ Medina, Adress: 326 Mueller, University Park, PA, 16801, USA; E-mail: [email protected]; http://orcid.org/0000-0001-5478-0522. Abstract Background: Anthozoa, Endocnidozoa, and Medusozoa are the 3 major clades of Cnidaria. Medusozoa is further divided into 4 clades, Hydrozoa, Staurozoa, Cubozoa, and Scyphozoa—the latter 3 lineages make up the clade Acraspeda. Acraspeda encompasses extraordinary diversity in terms of life history, numerous nuisance species, taxa with complex eyes rivaling other animals, and some of the most venomous organisms on the planet. Genomes have recently become available within Scyphozoa and Cubozoa, but there are currently no published genomes within Staurozoa and Cubozoa. Findings: Here we present 3 new draft genomes of Calvadosia cruxmelitensis (Staurozoa), Alatina alata (Cubozoa), and Cassiopea xamachana (Scyphozoa) for which we provide a preliminary orthology analysis that includes an inventory of their respective venom-related genes. Additionally, we identify synteny between POU and Hox genes that had previously been reported in a Received: 3 April 2018; Revised: 27 March 2019; Accepted: 21 May 2019 C The Author(s) 2019. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1 2 Draft genomes from diverse jellyfish (Cnidaria, Acraspeda) lineages hydrozoan, suggesting this linkage is highly conserved, possibly dating back to at least the last common ancestor of Medusozoa, yet likely independent of vertebrate POU-Hox linkages. Conclusions: These draft genomes provide a valuable resource for studying the evolutionary history and biology of these extraordinary animals, and for identifying genomic features underlying venom, vision, and life history traits in Acraspeda. Keywords: staurozoa; scyphozoa; cubozoa; acraspeda; cnidaria; medusozoa Introduction give rise to the medusoid form do so via lateral buds generated by asexual polyps, while others possess sexual polyps without Some of the most fascinating and outstanding mysteries related a free-swimming stage [28, 29]. Elsewhere within Cnidaria, An- to the genomic underpinnings of metazoan biology are centered Downloaded from https://academic.oup.com/gigascience/article-abstract/8/7/giz069/5524763 by guest on 03 July 2019 thozoa and the parasitic Endocnidozoa lack the medusa stage around cnidarians [1]. Active areas of research include the ba- or medusoid characters entirely. Research on medusa develop- sis of venom evolution and diversification [2–4], mechanisms of ment has shown similar gene expression patterns between hy- independent evolution of image-forming vision (lens eyes) [5– drozoans and scyphozoans, with developmental genes co-opted 7], and the emergence of a pelagic adult stage within a bipha- for patterning the medusa body plan [30, 31]. Interestingly, stro- sic (or multiphasic) life cycle [8]. Cnidaria encompasses 3 major bilation in scyphozoans was recently shown to be under the con- clades: Anthozoa, Endocnidozoa, and Medusozoa [9–12]. Antho- trol of the retinoic acid pathway [32–34]; these same genes are in- zoa comprises Hexacorallia and Octocorallia. Hexacorallia in- volved in metamorphosis of insects and amphibians, hinting to- cludes scleractinian corals, anemones, and zooanthids and is wards regulation of metamorphosis being a conserved function characterized by a 6-fold symmetry, with species exhibiting both in metazoans [35]. The study also found that potential lineage- colonial and solitary forms. Octocorallia includes sea fans, gor- specific genes were involved in controlling strobilation, sugges- gonians, and soft corals; these animals are characterized by pin- tive of genomic innovations within Medusozoa playing a role in nate tentacles in 8-fold symmetry. Endocnidozoa, comprising medusa morphogenesis, or more specifically within Scyphozoa. the parasitic lineages Myxozoa and Polypodiozoa, was only re- Hox genes, which control body formation during early em- cently properly classified as Cnidaria [13–15]. Medusozoans are bryonic development, predate the emergence of both Bilateria characterized by the emergence of a medusa life history stage and Cnidaria, and the evolution of these genes played a crucial within some taxa of the clade, their high diversity in regards to role in the diversification of these lineages [36–38]. In particu- life history and morphology, the presence of a linear mitochon- lar, clustering and synteny has been shown to be important in drial genome (with a variable number of chromosomes), and by bilaterians [39], but also in some cnidarians, such as the antho- the presence of a hinged cap at the apex of the cnidocyst (cnidar- zoan Nematostella vectensis [36, 40, 41], and in several hydrozoan ian stinging organelles) [8, 16, 17]. species [42–46]. Other than an initial characterization of select There are ∼3,900 described species within Medusozoa, classi- Hox genes in Cassiopea xamachana [47], information about Hox fied into 4 diverse lineages: Hydrozoa (hydroids, hydromedusae, genes and Hox gene clustering in Acraspeda species has been siphonophores), Staurozoa (stalked jellyfish), Cubozoa (box jel- limited. In hydrozoans and vertebrates, Hox genes were shown lyfish), and Scyphozoa (true jellyfish) (Fig. 1A−C) [1, 11]. There to be linked to another class of homeobox genes, the POU genes exists much debate regarding the phylogenetic relationships [48], but this linkage has not been demonstrated in any other among these lineages [10, 16, 18–20]. Recent phylogenomic anal- cnidarian lineages. These new Acraspeda genomes provide us yses have placed Staurozoa as the sister to a clade that con- with an opportunity to investigate the evolutionary history of tains Cubozoa and Scyphozoa, reuniting these lineages into a the POU-Hox linkage in more detail. group called Acraspeda (Fig. 1D) [9, 15, 21]. Given the exten- Genomic resources necessary to understand medusozoan sive morphological diversity within Cnidaria, understanding the evolution have been lacking, with genomes predominantly evolutionary relationships and mechanisms leading to lineage- available for anthozoans and hydrozoans [49–56]. However, 3 specific innovations has been of considerable interest but has new scyphozoan genomes, 2 genomes of the moon jellyfish Au- been fraught with challenges. In particular, the evolution and relia spp. and the giant Nomura’s jellyfish Nemopilema nomurai subsequent loss of the medusoid form in some lineages hints at were recently sequenced [57–59]. In addition, the genome for a complex evolutionary history within Medusozoa [22]. the cubozoan Morbakka virulenta has also recently been released The mechanisms of medusa formation are variable amongst [59]. While the majority of Medusozoa species are represented medusozoans, often involving 2 phenotypically distinct life by hydrozoans (>90%), both cubozoans and scyphozoans garner stages—polyp and medusa—that are genotypically identical (re- significant attention as a result of their impact on economy and viewed by Lewis Ames [1]). Cubozoan polyps undergo partial or tourism [1, 60]. Largely due to venom being used as a mecha- complete metamorphosis and develop into the adult medusoid nism of defense and prey capture, the inherent risk of jellyfish form capable of sexual reproduction, although in some cases sting has been exacerbated by uncertainty about how cnidar- a polyp rudiment remains [23]. Scyphozoan polyps (scyphis- ians will respond
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