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Evaluation of Genes Involved in Norway Lobster (Nephrops Norvegicus) Female Sexual Maturation Using Transcriptomic Analysis

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Evaluation of Genes Involved in Norway Lobster (Nephrops Norvegicus) Female Sexual Maturation Using Transcriptomic Analysis Hydrobiologia https://doi.org/10.1007/s10750-018-3521-3 CRUSTACEAN GENOMICS Evaluation of genes involved in Norway lobster (Nephrops norvegicus) female sexual maturation using transcriptomic analysis Guiomar Rotllant . Tuan Viet Nguyen . David Hurwood . Valerio Sbragaglia . Tomer Ventura . Joan B. Company . Silvia Joly . Abigail Elizur . Peter B. Mather Received: 6 October 2017 / Revised: 17 January 2018 / Accepted: 20 January 2018 Ó Springer International Publishing AG, part of Springer Nature 2018 Abstract The Norway lobster Nephrops norvegicus technology applied to multiple tissues. Ovarian mat- is the most important commercial crustacean species uration-related differential expression patterns were in Europe. Recent decline in wild captures and a observed for 4362 transcripts in ovary, hepatopan- reduction in total abundance and size at first matura- creas, eyestalk, brain, and thoracic ganglia in N. tion indicate that the species is overexploited. Increas- norvegicus. Transcripts detected in the study include ing knowledge of its reproduction, specifically at the vitellogenin, crustacean hyperglycaemic hormone, molecular level will be mandatory to improving retinoid X receptor, heat shock protein 90 and proteins fisheries management. The current study investigated encoding lipid and carbohydrate metabolizing differences between immature and mature N. norvegi- enzymes. From the study, data were collected that cus females using Next Generation Sequencing can prove valuable in developing more comprehensive knowledge of the reproductive system in this lobster species during the ovarian maturation process. Addi- Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10750-018-3521-3) con- tional studies will be required, however, to identify tains supplementary material, which is available to authorized potential novel genes and to develop a molecular users. toolkit for crustacean species that can be applied to improving sustainable future production. Guiomar Rotllant and Tuan Viet Nguyen have contributed equally to this work. Keywords Oocyte Á Fecundity Á Size at maturity Á Guest editors: Guiomar Rotllant, Ferran Palero, Peter Mather, Reproduction Á Fisheries Á Next generation sequencing Heather Bracken-Grissom & Begon˜a Santos / Crustacean Genomics G. Rotllant (&) Á J. B. Company Á S. Joly D. Hurwood Institut de Cie`ncies del Mar (ICM-CSIC), PasseigMarı´tim Earth, Environmental and Biological Sciences, Science de la Barceloneta 37-49, 08003 Barcelona, Spain and Engineering Faculty, Queensland University of e-mail: [email protected] Technology, 2 George St, Brisbane 4001, Australia T. V. Nguyen (&) Á T. Ventura Á A. Elizur P. B. Mather Faculty of Science, Health, Education and Engineering, Australian Rivers Institute, Griffith University, Nathan, GeneCology Research Centre, University of the Sunshine QLD 4111, Australia Coast, 4 Locked Bag, Maroochydore DC, QLD 4558, Australia e-mail: [email protected] 123 Hydrobiologia Introduction once but with immature ovaries) and had a CL of more than 24 mm (Rotllant et al., 2005) indicating a clear The Norway lobster Nephrops norvegicus (Linnaeus, reduction in size at first maturity (the study did not 1758) (Crustacea: Decapoda: Pleocyemata) has a wide calculate size at first maturity). distribution in European waters, including the conti- In light of N. norvegicus reproductive biology, a nental shelf and slope (4–754 m) in the Northeast number of studies have been conducted on morphol- Atlantic Ocean as far south as the Canary Islands and ogy of the reproductive system (Rotllant et al., Mediterranean Sea (Johnson et al., 2013). This con- 2005, 2012) and biochemical changes in the ovary stitutes one of the most important fisheries in Euro- (Rosa & Nunes, 2002). These insights included pean waters while being the most valuable harvested characterization of vitellogenin activity (Vg; Rotllant crustacean in the region. This species is closely et al., 2017) and gonad inhibiting hormone (GIH; monitored by the International Council for the Explo- Edomi et al., 2002) and other crustacean hyper- ration of the Sea (ICES) under the Working Group on glycemic hormones (CHH; Mettulio et al., 2004). In Nephrops Surveys (http://www.ices.dk/community/ crustaceans, oocyte development includes a series of groups/Pages/WGNEPS.aspx). Reproduction takes complex cellular events, and different genes are place either biannually (Iceland) or annually involved that control developmental stage and storage (Mediterranean Sea). During this period, females carry of proteins for embryogenesis (Subramoniam, 2011). eggs on their abdomen after fertilization from sperm Recently, genes that have a potent role in reproduction deposited previously by a male during copulation. and development have been identified in a number of Sperm is stored in the female’s thelycum until crustaceans notably in shrimp, prawns, lobsters, ` spawning takes place (Sarda, 1995). In the Catalan crayfishes, and crabs (Wong et al., 2008; Wu & Chu, region (Western Mediterranean Sea), oocyte matura- 2008; Wu et al., 2009; Zeng et al., 2011; Brady et al., tion commences in spring, a single spawning event 2012, 2013; Jiang et al., 2014; Wang et al., 2014; occurs in summer and females carry eggs on their Rotllant et al., 2015; Saetan et al., 2016). As an abdomen until eggs hatch in the following early spring example, genes that were differentially expressed (Rotllant et al., 2005). Prior to this, ovaries remain between immature and mature females have been immature while females carry eggs. A steady decline identified in the ovary of black tiger shrimp Penaeus in the N. norvegicus population has been reported in monodon Fabricius, 1798 (Brady et al., 2013) and the Catalan region over 20 years (27% decline) even banana shrimp Fenneropenaeus merguiensis (de Man, though total trawler activity has diminished 28% and 1888) (Saetan et al., 2016), hepatopancreas of the cod-end mesh size has been increased from 36–38 to shrimp Metapenaeus ensis (De Haan, 1844) (Wong ` 40 mm (Sarda, 1998). Additionally, mean size of et al., 2008) and the swimming crab Portunus Norway lobster individuals has decreased from 4 mm trituberculatus (Miers, 1876) (Wang et al., 2014), carapace length (CL) in males to 3.6 mm CL in cephalothorax and eyestalks of P. monodon (Brady females (a difference of approximately 25%). This et al., 2012) and thoracic ganglia in the mud crab corresponds to a reduction of 1–2 years in age of Scylla paramamosain Estampador, 1950 (Zeng et al., captured individuals. Thus, current exploitation is 2011). Notably transcripts that encode vitellogenin directed at younger individuals closer to size at first (the major egg yolk protein), vitellogenin receptor reproduction event and will remove a substantial (VgR), lipid and carbohydrate metabolism related ` proportion of the spawning stock. Sarda (1991) proteins, C-type lectins (CTLs), and hemocyanins determined size at which 50% of individuals reach have also been identified. their first maturity for females at 30–31 mm CL. Ten In the current study, we employed RNA-sequenc- years later however, a study conducted in the same ing technology to investigate genes involved in sexual area resulted in no females being captured in stage II maturation in N. norvegicus. To our knowledge, this is (adult females that have already reproduced at least the first study that compares multi-tissue transcrip- tomes using Next Generation Sequencing (NGS) from V. Sbragaglia immature and mature females in decapods to under- Department of Biology and Ecology of Fishes, Leibniz- Institute of Freshwater Ecology and Inland Fisheries, stand the molecular mechanism controlling ovarian Mu¨ggelseedamm, 310, Berlin, Germany development. Knowledge of mechanisms governing 123 Hydrobiologia ovarian development processes at the molecular level Table 2 De novo assembly statistics of the N. norvegicus will be valuable not only to expand the molecular reference transcriptome (Rotllant et al., 2017) toolkit available for N. norvegicus in the near future, Number of contig 333,225 but can also serve as reference information for other Total size of transcript (nt) 235,992,830 related crustacean species. N50 (bp) 1272 Longest transcripts (bp) 33,925 Mean transcript size (bp) 708 Materials and methods Reference transcriptome Bioinformatics The current study used a reference transcriptome generated previously (Rotllant et al., 2017). RNA-seq For downstream analysis, quality-trimmed reads from statistics are summarized in Tables 1 and 2. In brief, all immature and mature female tissue samples were female N. norvegicus were collected offshore from mapped back to the previously generated reference Barcelona harbor (Spain). In the laboratory, large transcriptome assembly using Bowtie (Parra et al., females (CL = 34.3 ± 2.1 mm; total wet 2007). Reads counting was generated using RSEM (Li weight = 26.0 ± 5.0 mg) were selected and classi- & Dewey, 2011). Fragments per kilobase of transcript fied following their maturation stage (Rotllant et al., per million mapped reads value (FPKM) were 2005) as immature [stage II; Gonado-somatic index recorded. Following this, EdgeR software (Ye et al., (GSI) = 1.02 ± 0.17] and mature (stage IV; 2006) was used to measure false discovery rate of GSI = 1.91 ± 0.18). No difference in hepato-somatic multiple-hypothesis testing. Designated threshold for indexes (HIS) between immature and mature females any genes to be confirmed as significantly different was identified (HIS = 4.27 ± 0.68). Tissues (ovaries,
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