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    Author
    Ravasi, Timothy (10)
    Voolstra, Christian R. (6)Berumen, Michael L. (5)Ryu, Tae Woo (5)Aranda, Manuel (3)View MoreDepartmentBiological and Environmental Sciences and Engineering (BESE) Division (10)
    Bioscience Program (10)
    Marine Science Program (10)Red Sea Research Center (RSRC) (10)Computational Bioscience Research Center (CBRC) (8)View MoreJournalNature Climate Change (2)Scientific Reports (2)BMC Genomics (1)Ecology and Evolution (1)Environmental Microbiology (1)View MoreKAUST Acknowledged Support UnitAcademic Writing (1)Coastal and Marine Laboratory (1)Core Labs (1)KAUST Grant NumberSA-00040/UKC0016 (1)PublisherSpringer Nature (6)Wiley (3)Oxford University Press (OUP) (1)SubjectStylissa carteri (2)allele (1)Animal proteomics (1)Bugula neritina (1)Connectivity (1)View MoreTypeArticle (10)Year (Issue Date)2017 (1)2016 (4)2015 (1)2014 (1)2013 (2)View MoreItem AvailabilityOpen Access (6)Metadata Only (4)

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    Rapid adaptive responses to climate change in corals

    Torda, Gergely; Donelson, Jennifer M.; Aranda, Manuel; Barshis, Daniel J.; Bay, Line; Berumen, Michael L.; Bourne, David G.; Cantin, Neal; Foret, Sylvain; Matz, Mikhail; Miller, David J.; Moya, Aurelie; Putnam, Hollie M.; Ravasi, Timothy; van Oppen, Madeleine J. H.; Thurber, Rebecca Vega; Vidal-Dupiol, Jeremie; Voolstra, Christian R.; Watson, Sue-Ann; Whitelaw, Emma; Willis, Bette L.; Munday, Philip L. (Nature Climate Change, Springer Nature, 2017-09-01) [Article]
    Pivotal to projecting the fate of coral reefs is the capacity of reef-building corals to acclimatize and adapt to climate change. Transgenerational plasticity may enable some marine organisms to acclimatize over several generations and it has been hypothesized that epigenetic processes and microbial associations might facilitate adaptive responses. However, current evidence is equivocal and understanding of the underlying processes is limited. Here, we discuss prospects for observing transgenerational plasticity in corals and the mechanisms that could enable adaptive plasticity in the coral holobiont, including the potential role of epigenetics and coral-associated microbes. Well-designed and strictly controlled experiments are needed to distinguish transgenerational plasticity from other forms of plasticity, and to elucidate the underlying mechanisms and their relative importance compared with genetic adaptation.
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    Novel polymorphic microsatellite markers developed for a common reef sponge, Stylissa carteri

    Giles, Emily; Saenz Agudelo, Pablo; Berumen, Michael L.; Ravasi, Timothy (Marine Biodiversity, Springer Nature, 2013-04-04) [Article]
    Despite the ubiquitous role sponges play in reef ecosystem dynamics, little is known about population-level connectivity in these organisms. The general field of population genetics in sponges remains in its infancy. To date, microsatellite markers have only been developed for few sponge species and no sponge population genetics studies using microsatellites have been conducted in the Red Sea. Here, with the use of next-generation sequencing, we characterize 12 novel polymorphic loci for the common reef sponge, Stylissa carteri. The number of alleles per loci ranged between three and eight. Observed heterozygosity frequencies (Ho) ranged from 0.125 to 0.870, whereas expected (He) heterozygosity frequencies ranged from 0.119 to 0.812. Only one locus showed consistent deviations from Hardy-Weinberg equilibrium (HWE) in both populations and two loci consistently showed the possible presence of null alleles. No significant linkage disequilibrium was detected for any pairs of loci. These microsatellites will be of use for numerous ecological studies focused on this common and abundant sponge. 2013 The Author(s).
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    Revealing microbial functional activities in the Red Sea sponge S tylissa carteri by metatranscriptomics

    Moitinho-Silva, Lucas; Seridi, Loqmane; Ryu, Tae Woo; Voolstra, Christian R.; Ravasi, Timothy; Hentschel, Ute (Environmental Microbiology, Wiley, 2014-07-09) [Article]
    The persistence of coral reef ecosystems relies on the symbiotic relationship between scleractinian corals and intracellular, photosynthetic dinoflagellates in the genus Symbiodinium. Genetic evidence indicates that these symbionts are biologically diverse and exhibit discrete patterns of environmental and host distribution. This makes the assessment of Symbiodinium diversity critical to understanding the symbiosis ecology of corals. Here, we applied pyrosequencing to the elucidation of Symbiodinium diversity via analysis of the internal transcribed spacer 2 (ITS2) region, a multicopy genetic marker commonly used to analyse Symbiodinium diversity. Replicated data generated from isoclonal Symbiodinium cultures showed that all genomes contained numerous, yet mostly rare, ITS2 sequence variants. Pyrosequencing data were consistent with more traditional denaturing gradient gel electrophoresis (DGGE) approaches to the screening of ITS2 PCR amplifications, where the most common sequences appeared as the most intense bands. Further, we developed an operational taxonomic unit (OTU)-based pipeline for Symbiodinium ITS2 diversity typing to provisionally resolve ecologically discrete entities from intragenomic variation. A genetic distance cut-off of 0.03 collapsed intragenomic ITS2 variants of isoclonal cultures into single OTUs. When applied to the analysis of field-collected coral samples, our analyses confirm that much of the commonly observed Symbiodinium ITS2 diversity can be attributed to intragenomic variation. We conclude that by analysing Symbiodinium populations in an OTU-based framework, we can improve objectivity, comparability and simplicity when assessing ITS2 diversity in field-based studies.
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    Sex Change in Clownfish: Molecular Insights from Transcriptome Analysis

    Castano, Laura Casas; Saborido-Rey, Fran; Ryu, Tae Woo; Michell, Craig; Ravasi, Timothy; Irigoien, Xabier (Scientific Reports, Springer Nature, 2016-10-17) [Article]
    Sequential hermaphroditism is a unique reproductive strategy among teleosts that is displayed mainly in fish species living in the coral reef environment. The reproductive biology of hermaphrodites has long been intriguing; however, very little is known about the molecular pathways underlying their sex change. Here, we provide the first de novo transcriptome analyses of a hermaphrodite teleost´s undergoing sex change in its natural environment. Our study has examined relative gene expression across multiple groups—rather than just two contrasting conditions— and has allowed us to explore the differential expression patterns throughout the whole process. Our analysis has highlighted the rapid and complex genomic response of the brain associated with sex change, which is subsequently transmitted to the gonads, identifying a large number of candidate genes, some well-known and some novel, involved in the process. The present study provides strong evidence of the importance of the sex steroidogenic machinery during sex change in clownfish, with the aromatase gene playing a central role, both in the brain and the gonad. This work constitutes the first genome-wide study in a social sex-changing species and provides insights into the genetic mechanism governing social sex change and gonadal restructuring in protandrous hermaphrodites.
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    Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

    Aranda, Manuel; Li, Yangyang; Liew, Yi Jin; Baumgarten, Sebastian; Simakov, O.; Wilson, M. C.; Piel, J.; Ashoor, Haitham; Bougouffa, Salim; Bajic, Vladimir B.; Ryu, Tae Woo; Ravasi, Timothy; Bayer, Till; Micklem, G.; Kim, H.; Bhak, J.; LaJeunesse, T. C.; Voolstra, Christian R. (Scientific Reports, Springer Nature, 2016-12-22) [Article]
    Despite half a century of research, the biology of dinoflagellates remains enigmatic: they defy many functional and genetic traits attributed to typical eukaryotic cells. Genomic approaches to study dinoflagellates are often stymied due to their large, multi-gigabase genomes. Members of the genus Symbiodinium are photosynthetic endosymbionts of stony corals that provide the foundation of coral reef ecosystems. Their smaller genome sizes provide an opportunity to interrogate evolution and functionality of dinoflagellate genomes and endosymbiosis. We sequenced the genome of the ancestral Symbiodinium microadriaticum and compared it to the genomes of the more derived Symbiodinium minutum and Symbiodinium kawagutii and eukaryote model systems as well as transcriptomes from other dinoflagellates. Comparative analyses of genome and transcriptome protein sets show that all dinoflagellates, not only Symbiodinium, possess significantly more transmembrane transporters involved in the exchange of amino acids, lipids, and glycerol than other eukaryotes. Importantly, we find that only Symbiodinium harbor an extensive transporter repertoire associated with the provisioning of carbon and nitrogen. Analyses of these transporters show species-specific expansions, which provides a genomic basis to explain differential compatibilities to an array of hosts and environments, and highlights the putative importance of gene duplications as an evolutionary mechanism in dinoflagellates and Symbiodinium.
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    Molecular signatures of transgenerational response to ocean acidification in a species of reef fish

    Schunter, Celia Marei; Welch, Megan J.; Ryu, Tae Woo; Zhang, Huoming; Berumen, Michael L.; Nilsson, Göran E.; Munday, Philip L.; Ravasi, Timothy (Nature Climate Change, Springer Nature, 2016-08-01) [Article]
    The impact of ocean acidification on marine ecosystems will depend on species capacity to adapt. Recent studies show that the behaviour of reef fishes is impaired at projected CO levels; however, individual variation exists that might promote adaptation. Here, we show a clear signature of parental sensitivity to high CO in the brain molecular phenotype of juvenile spiny damselfish, Acanthochromis polyacanthus, primarily driven by circadian rhythm genes. Offspring of CO -tolerant and CO -sensitive parents were reared at near-future CO (754 μatm) or present-day control levels (414 μatm). By integrating 33 brain transcriptomes and proteomes with a de novo assembled genome we investigate the molecular responses of the fish brain to increased CO and the expression of parental tolerance to high CO in the offspring molecular phenotype. Exposure to high CO resulted in differential regulation of 173 and 62 genes and 109 and 68 proteins in the tolerant and sensitive groups, respectively. Importantly, the majority of differences between offspring of tolerant and sensitive parents occurred in high CO conditions. This transgenerational molecular signature suggests that individual variation in CO sensitivity could facilitate adaptation of fish populations to ocean acidification.
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    Hologenome analysis of two marine sponges with different microbiomes

    Ryu, Tae Woo; Seridi, Loqmane; Moitinho-Silva, Lucas; Oates, Matthew; Liew, Yi Jin; Mavromatis, Charalampos Harris; Wang, Xiaolei; Haywood, Annika; Lafi, Feras Fawzi; Kupresanin, Marija; Sougrat, Rachid; Alzahrani, Majed A.; Giles, Emily; Ghosheh, Yanal; Schunter, Celia Marei; Baumgarten, Sebastian; Berumen, Michael L.; Gao, Xin; Aranda, Manuel; Foret, Sylvain; Gough, Julian; Voolstra, Christian R.; Hentschel, Ute; Ravasi, Timothy (BMC Genomics, Springer Nature, 2016-02-29) [Article]
    Background Sponges (Porifera) harbor distinct microbial consortia within their mesohyl interior. We herein analysed the hologenomes of Stylissa carteri and Xestospongia testudinaria, which notably differ in their microbiome content. Results Our analysis revealed that S. carteri has an expanded repertoire of immunological domains, specifically Scavenger Receptor Cysteine-Rich (SRCR)-like domains, compared to X. testudinaria. On the microbial side, metatranscriptome analyses revealed an overrepresentation of potential symbiosis-related domains in X. testudinaria. Conclusions Our findings provide genomic insights into the molecular mechanisms underlying host-symbiont coevolution and may serve as a roadmap for future hologenome analyses.
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    Exploring seascape genetics and kinship in the reef sponge Stylissa carteri in the Red Sea

    Giles, Emily; Saenz Agudelo, Pablo; Hussey, Nigel E.; Ravasi, Timothy; Berumen, Michael L. (Ecology and Evolution, Wiley, 2015-06-01) [Article]
    A main goal of population geneticists is to study patterns of gene flow to gain a better understanding of the population structure in a given organism. To date most efforts have been focused on studying gene flow at either broad scales to identify barriers to gene flow and isolation by distance or at fine spatial scales in order to gain inferences regarding reproduction and local dispersal. Few studies have measured connectivity at multiple spatial scales and have utilized novel tools to test the influence of both environment and geography on shaping gene flow in an organism. Here a seascape genetics approach was used to gain insight regarding geographic and ecological barriers to gene flow of a common reef sponge, Stylissa carteri in the Red Sea. Furthermore, a small-scale (<1 km) analysis was also conducted to infer reproductive potential in this organism. At the broad scale, we found that sponge connectivity is not structured by geography alone, but rather, genetic isolation in the southern Red Sea correlates strongly with environmental heterogeneity. At the scale of a 50-m transect, spatial autocorrelation analyses and estimates of full-siblings revealed that there is no deviation from random mating. However, at slightly larger scales (100–200 m) encompassing multiple transects at a given site, a greater proportion of full-siblings was found within sites versus among sites in a given location suggesting that mating and/or dispersal are constrained to some extent at this spatial scale. This study adds to the growing body of literature suggesting that environmental and ecological variables play a major role in the genetic structure of marine invertebrate populations.
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    The Global Invertebrate Genomics Alliance (GIGA): Developing Community Resources to Study Diverse Invertebrate Genomes

    Bracken-Grissom, Heather; Collins, Allen G.; Collins, Timothy; Crandall, Keith; Distel, Daniel; Dunn, Casey; Giribet, Gonzalo; Haddock, Steven; Knowlton, Nancy; Martindale, Mark; Medina, Monica; Messing, Charles; O'Brien, Stephen J.; Paulay, Gustav; Putnam, Nicolas; Ravasi, Timothy; Rouse, Greg W.; Ryan, Joseph F.; Schulze, Anja; Worheide, Gert; Adamska, Maja; Bailly, Xavier; Breinholt, Jesse; Browne, William E.; Diaz, M. Christina; Evans, Nathaniel; Flot, Jean-Francois; Fogarty, Nicole; Johnston, Matthew; Kamel, Bishoy; Kawahara, Akito Y.; Laberge, Tammy; Lavrov, Dennis; Michonneau, Francois; Moroz, Leonid L.; Oakley, Todd; Osborne, Karen; Pomponi, Shirley A.; Rhodes, Adelaide; Rodriguez-Lanetty, Mauricio; Santos, Scott R.; Satoh, Nori; Thacker, Robert W.; Van de Peer, Yves; Voolstra, Christian R.; Welch, David Mark; Winston, Judith; Zhou, Xin (Journal of Heredity, Oxford University Press (OUP), 2013-12-11) [Article]
    Over 95% of all metazoan (animal) species comprise the invertebrates, but very few genomes from these organisms have been sequenced. We have, therefore, formed a Global Invertebrate Genomics Alliance (GIGA). Our intent is to build a collaborative network of diverse scientists to tackle major challenges (e.g., species selection, sample collection and storage, sequence assembly, annotation, analytical tools) associated with genome/transcriptome sequencing across a large taxonomic spectrum. We aim to promote standards that will facilitate comparative approaches to invertebrate genomics and collaborations across the international scientific community. Candidate study taxa include species from Porifera, Ctenophora, Cnidaria, Placozoa, Mollusca, Arthropoda, Echinodermata, Annelida, Bryozoa, and Platyhelminthes, among others. GIGA will target 7000 noninsect/nonnematode species, with an emphasis on marine taxa because of the unrivaled phyletic diversity in the oceans. Priorities for selecting invertebrates for sequencing will include, but are not restricted to, their phylogenetic placement; relevance to organismal, ecological, and conservation research; and their importance to fisheries and human health. We highlight benefits of sequencing both whole genomes (DNA) and transcriptomes and also suggest policies for genomic-level data access and sharing based on transparency and inclusiveness. The GIGA Web site () has been launched to facilitate this collaborative venture.
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    Rapid transcriptome and proteome profiling of a non-model marine invertebrate, Bugula neritina

    Wang, Hao; Zhang, Huoming; Wong, Yuehim; Voolstra, Christian R.; Ravasi, Timothy; Bajic, Vladimir B.; Qian, Pei-Yuan (PROTEOMICS, Wiley, 2010-06-10) [Article]
    Non-model organisms represent the majority of life forms in our planet. However, the lack of genetic information hinders us to understand the unique biological phenomena in non-model organisms at the molecular level. In this study, we applied a tandem transcriptome and proteome profiling on a non-model marine fouling organism, Bugula neritina. Using a 454 pyrosequencing platform with the updated titanium reagents, we generated a total of 48M bp transcriptome data consisting of 131 450 high-quality reads. Of these, 122 650 reads (93%) were assembled to produce 6392 contigs with an average length of 538 bases and the remaining 8800 reads were singletons. Of the total 15 192 unigenes, 13 863 ORFs were predicated, of which 6917 were functionally annotated based on gene ontology and eukaryotic orthologous groups. Subsequent proteome analysis identified and quantified 882 proteins from B. neritina. These results would provide fundamental and important information for the subsequent studies of molecular mechanism in larval biology, development, antifouling research. Furthermore, we demonstrated, for the first time, the combined use of two high-throughput technologies as a powerful approach for accelerating the studies of non-model but otherwise important species. © 2010 Wiley-VCH Verlag GmbH & Co. KGaA.
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