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- SuperSAGE digital expression analysis of differential growth rate in a European sea bass populationPublication . Louro, Bruno; Martins, Rute S.T.; Pinto, Patricia IS; Reinhardt, Richard; de Koning, Dirk-Jan; Canario, Adelino; Power, DeborahOne of the goals of the aquaculture industry is to understand and control growth associated traits through selective breeding. In the present study the molecular basis of growth heterogeneity in the European sea bass (Dicentrarchus labrax) was addressed. To establish growth heterogeneity in a group of hatchery bred sea bass individuals were tagged and their specific growth rates (SGR) determined at monthly intervals. Gene expression in the brain, liver and white muscle from fish with the most divergent sustained SGR (6 individuals of the first and last quartile) was assessed using SuperSAGE (Serial Analysis Gene Expression) combined with next generation SOLiD4 sequencing. A total of approx. 11 million edited tags (26 bp), on average 2 million tags per SAGE library, that represented 47.071 unique transcripts were identified. Comparison of transcripts in fish with high and low SGR yielded 344, 698 and 601 differently expressed tags (0.01% false discovery rate and 4-fold change) in brain, liver and muscle, respectively. The tags were mapped onto the sea bass genome and approximately one third of the tags could be assigned to annotated genes. Pathway enrichment analysis revealed in liver, muscle and brain intricate gene expression changes in endocrine regulatory pathways involved in growth, metabolic and the stress axis, underlying divergent SGR in sea bass.
- Transcriptomic down-regulation of immune system components in barrier and hematopoietic tissues after lipopolysaccharide injection in antarctic notothenia coriicepsPublication . Sousa, Carmen; Power, Deborah; Guerreiro, Pedro M; Louro, Bruno; Chen, Liangbiao; Canario, AdelinoThe environmental conditions and isolation in the Antarctic have driven the evolution of a unique biodiversity at a macro to microorganism scale. Here, we investigated the possible adaptation of the teleost Notothenia coriiceps immune system to the cold environment and unique microbial community of the Southern Ocean. The fish immune system was stimulated through an intraperitoneal injection of lipopolysaccharide (LPS 0111:B4 from E. coli) and the tissue transcriptomic response and plasma biochemistry were analyzed 7 days later and compared to a sham injected control. Gene transcription in the head-kidney, intestine and skin was significantly modified by LPS, although tissues showed different responsiveness, with the duodenum most modified and the skin the least modified. The most modified processes in head-kidney, duodenum and skin were related to cell metabolism (up-regulated) and the immune system (comprising 30% of differentially expressed genes). The immune processes identified were mostly down-regulated, particularly interleukins and pattern recognition receptors (PRRs), nucleotide-binding oligomerization domain-like receptors and mannose receptors, unlike the toll-like receptors response commonly described in other teleost fish. The modified transcriptional response was not mirrored by a modified systemic response, as the circulating levels of enzymes of innate immunity, lysozyme and antiproteases, were not significantly different from the untreated and sham control fish. In conclusion, while the N. coriiceps immune system shares many features with other teleosts there are also some specificities. Further studies should better characterize the PRRs and their role in Antarctic teleosts, as well as the importance of the LPS source and its consequences for immune activation in teleosts.
- A new subfamily of ionotropic glutamate receptors unique to the echinoderms with putative sensory rolePublication . Sania, Rubaiyat E.; Cardoso, João; Louro, Bruno; Marquet, Nathalie; Canario, AdelinoChemosensation is a critical signalling process in animals and especially important in sea cucumbers, a group of ecologically and economically important marine echinoderms (class Holothuroidea), which lack audio and visual organs and rely on chemical sensing for survival, feeding and reproduction. The ionotropic receptors are a recently identified family of chemosensory receptors in insects and other protostomes, related to the ionotropic glutamate receptor family (iGluR), a large family of membrane receptors in metazoan. Here we characterize the echinoderm iGluR subunits and consider their possible role in chemical communication in sea cucumbers. Sequence similarity searches revealed that sea cucumbers have in general a higher number of iGluR subunits when compared to other echinoderms. Phylogenetic analysis and sequence comparisons revealed GluH as a specific iGluR subfamily present in all echinoderms. Homologues of the vertebrate GluA (aka alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid, AMPA), GluK (aka kainate) and GluD (aka delta) were also identified. The GluN (aka N-methyl-d-aspartate, NMDA) as well as the invertebrate deuterostome subfamily GluF (aka phi) are absent in echinoderms. The echinoderm GluH subfamily shares conserved structural protein organization with vertebrate iGluRs and the ligand binding domain (LBD) is the most conserved region; genome analysis indicates evolution via lineage and species-specific tandem gene duplications. GluH genes (named Grih) are the most highly expressed iGluRs subunit genes in tissues in the sea cucumber Holothuria arguinesis, with Griha1, Griha2 and Griha5 exclusively expressed in tentacles, making them candidates to have a chemosensory role in this species. The multiple GluH subunits may provide alternative receptor assembly combinations, thus expanding the functional possibilities and widening the range of compounds detected during aggregation and spawning in echinoderms.
- Transcriptomics reveals that the caudal neurosecretory system in the olive flounder (Paralichthys olivaceus) is more responsive in bold individuals and to chronic temperature changePublication . Yuan, Mingzhe; Zhang, Xueshu; Louro, Bruno; Li, Xiaoxue; Canario, Adelino; Lu, WeiqunIn farmed animals, personalities have demonstrated links to performance traits, health and welfare, disease susceptibility, and to coping with environmental stress. The teleost caudal neurosecretory system (CNSS) of the posterior spinal cord is involved in the regulation of the osmoregulatory and stress responses and can directly sense a hypothermal challenge via a transient receptor potential ion channel. Here we investigated the global transcriptomic response of the CNSS of shy and bold individuals of the olive flounder (Paralichthys olivaceus) acclimated to 18 degrees C and transferred to 12 degrees C (low temperature treatment, LT) or 24 degrees C (high temperature treatment, HT) for 2 h (acute) or 8 days (chronic) in relation to fish maintained at 18 degrees C (control). Overall, differential transcriptomic responses were stronger in bold individuals and induced by acute HT and chronic LT treatments. Acute HT induced innate immunity, circadian rhythm, and cellular stress response pathways and, specifically in bold individuals, a heightened response of molecular chaperones of cellular response to heat which may be related to the mechanisms of rescue of downregulated RNA splicing processes. Chronic LT also caused downregulation of innate immunity pathways as well as pathways related to cell division. In addition, the CNSS of bold individuals was enriched in pathways related to regulation of cell cycle, adaptive immune response, and apoptosis, while cellular metabolism pathways were downregulated in shy individuals. The putative temperature sensor genes Trpv1 and Trpa1 were upregulated, respectively, after acute HT and chronic LT treatments, but there was no indication of a specific neurosecretory response of the CNSS. While several of the observed transcriptomic responses to temperature appear to be shared by other tissues and species, it is also clear that bold and shy behavioural personalities show marked different responses, with bold individuals the most responsive. These results add to the knowledge base available on olive flounder aquaculture, indicating a differential role of the CNSS in the response to temperature change according to behavioural personalities.
- Genomic analysis of Sparus aurata reveals the evolutionary dynamics of sex-biased genes in a sequential hermaphrodite fishPublication . Pauletto, Marianna; Manousaki, Tereza; Ferraresso, Serena; Babbucci, Massimiliano; Tsakogiannis, Alexandros; Louro, Bruno; Vitulo, Nicola; Quoc, Viet Ha; Carraro, Roberta; Bertotto, Daniela; Franch, Rafaella; Maroso, Francesco; Aslam, Muhammad L.; Sonesson, Anna K.; Simionati, Barbara; Malacrida, Giorgio; Cestaro, Alessandro; Caberlotto, Stefano; Sarropoulou, Elena; Mylonas, Costantinos C.; Power, Deborah; Patarnello, Tomaso; Canario, Adelino; Tsigenopoulos, Costas; Bargelloni, LucaSexual dimorphism is a fascinating subject in evolutionary biology and mostly results from sex-biased expression of genes, which have been shown to evolve faster in gonochoristic species. We report here genome and sex-specific transcriptome sequencing of Sparus aurata, a sequential hermaphrodite fish. Evolutionary comparative analysis reveals that sex-biased genes in S. aurata are similar in number and function, but evolved following strikingly divergent patterns compared with gonochoristic species, showing overall slower rates because of stronger functional constraints. Fast evolution is observed only for highly ovary-biased genes due to female-specific patterns of selection that are related to the peculiar reproduction mode of S. aurata, first maturing as male, then as female. To our knowledge, these findings represent the first genome-wide analysis on sex-biased loci in a hermaphrodite vertebrate species, demonstrating how having two sexes in the same individual profoundly affects the fate of a large set of evolutionarily relevant genes.
- Holothurians have a reduced GPCR and odorant receptor-like repertoire compared to other echinodermsPublication . Marquet, Nathalie; Cardoso, João CR; Louro, Bruno; Fernandes, Stefan; Silva, Sandra; Canario, AdelinoSea cucumbers lack vision and rely on chemical sensing to reproduce and survive. However, how they recognize and respond to environmental cues remains unknown. Possible candidates are the odorant receptors (ORs), a diverse family of G protein-coupled receptors (GPCRs) involved in olfaction. The present study aimed at characterizing the chemosensory GPCRs in sea cucumbers. At least 246 distinct GPCRs, of which ca. 20% putative ORs, were found in a transcriptome assembly of putative chemosensory (tentacles, oral cavity, calcareous ring, and papillae/tegument) and reproductive (ovary and testis) tissues from Holothuria arguinensis (57 ORs) and in the Apostichopus japonicus genome (79 ORs). The sea cucumber ORs clustered with those of sea urchin and starfish into four main clades of gene expansions sharing a common ancestor and evolving under purifying selection. However, the sea cucumber ORs repertoire was the smallest among the echinoderms and the olfactory receptor signature motif LxxPxYxxxxxLxxxDxxxxxxxxP was better conserved in cluster OR-l1 which also had more members. ORs were expressed in tentacles, oral cavity, calcareous ring, and papillae/tegument, supporting their potential role in chemosensing. This study is the first comprehensive survey of chemosensory GPCRs in sea cucumbers, and provides the molecular basis to understand how they communicate.
- Characterization and refinement of growth related quantitative trait loci in European sea bass (Dicentrarchus labrax) using a comparative approachPublication . Louro, Bruno; Kuhl, Heiner; Tine, Mbaye; de Koning, Dirk-Jan; Batargias, Costas; Volckaert, Filip A. M.; Reinhardt, Richard; Canario, Adelino; Power, DeborahThe identification of genetic markers for traits of interest for aquaculture, such as growth, is an important step for the establishment of breeding programmes. As more genomic information becomes available the possibility of applying comparative genomics to identify and refine quantitative trait locus (QTLs) and potentially identify candidate genes responsible for the QTL effect may accelerate genetic improvement in established and new aquaculture species. Here we report such an approach on growth related traits in the European sea bass (Dicentrarchus labrax), an important species for European aquaculture. A genetic map was generated with markers targeted to previously identified QTL for growth which reduced distance and improved resolution in these regions. A total of 36 significant QTLs were identified when morphometric traits were considered individually in maternal half sibs, paternal half sibs and sib-pair analysis. Twenty seven new markers targeted to the growth QTLs, obtained by comparative mapping, reduced the average distance between markers from 23.4, 9.1, and 5.8 cM in the previous map to 3.4, 2.2, and 5.2 cM, on linkage group (LG) LG4, LG6 and LG15 respectively. Lists of genes embedded in the QTL - 591 genes in LG4, 234 genes in LG6 and 450 genes in LG15 - were obtained from the European sea bass genome. Comparative mapping revealed conserved gene synteny across teleost fishes. Functional protein association network analysis with the gene products of the 3 linkage groups revealed a large global association network including 42 gene products. Strikingly the association network was populated with genes of known biological importance for growth and body weight in terrestrial farm animals, such as elements of the signaling pathways for Jak-STAT, MAPK, adipocytokine and insulin, growth hormone, IGFI and II. This study demonstrates the feasibility of a comparative genomics combined with functional gene annotation to refine the resolution of QTL and the establishment of hypothesis to accelerate discovery of putative responsible genes.Statement of relevance: This study demonstrates the feasibility of a comparative genomics approach, combined with functional annotation to refine the resolution of QTL and establishment of hypothesis to accelerate discovery of candidate genes. As production of genomic data is becoming more accessible, the implementation of this strategy will rapidly and efficiently provide the tools required for genetic selection in new candidate aquaculture species. (C) 2016 Elsevier B.V. All rights reserved.