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    Aranda, Manuel (12)
    Voolstra, Christian R. (8)Liew, Yi Jin (6)Li, Yong (4)Baumgarten, Sebastian (3)View MoreDepartmentBiological and Environmental Sciences and Engineering (BESE) Division (12)Marine Science Program (12)Red Sea Research Center (RSRC) (12)Bioscience Program (4)Computational Bioscience Research Center (CBRC) (2)View MoreJournalMolecular Ecology Resources (2)BMC Microbiology (1)Frontiers in Marine Science (1)Genome Biology and Evolution (1)Molecular Ecology (1)View MoreKAUST Grant NumberCRG-1-2012-BER-002 (1)URF/1/1705-01 (1)PublisherSpringer Nature (4)Wiley (3)Cold Spring Harbor Laboratory (1)Dryad Digital Repository (1)Frontiers Media SA (1)View MoreSubjectCorallimorpharia (2)Adaptation (1)adaptation (1)Aiptasia (1)Amplexidiscus Fenestrafer (1)View MoreTypeArticle (10)Dataset (1)Preprint (1)Year (Issue Date)
    2017 (12)
    Item AvailabilityOpen Access (10)Metadata Only (2)

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    Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals

    Voolstra, Christian R.; Li, Yong; Liew, Yi Jin; Baumgarten, Sebastian; Zoccola, Didier; Flot, Jean-François; Tambutté, Sylvie; Allemand, Denis; Aranda, Manuel (Scientific Reports, Springer Nature, 2017-12-08) [Article]
    Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary divergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata, and compared it to the available genome of a complex coral, Acropora digitifera. We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Genes associated with the algal symbiosis were also independently expanded in both species, but both corals diverged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Future analyses incorporating more genomic data should be able to determine whether the patterns elucidated here are not only characteristic of the differences between S. pistillata and A. digitifera but also representative of corals from the robust and complex clade at large.
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    Laboratory-Cultured Strains of the Sea Anemone Exaiptasia Reveal Distinct Bacterial Communities

    Herrera Sarrias, Marcela; Ziegler, Maren; Voolstra, Christian R.; Aranda, Manuel (Frontiers in Marine Science, Frontiers Media SA, 2017-05-02) [Article]
    Exaiptasia is a laboratory sea anemone model system for stony corals. Two clonal strains are commonly used, referred to as H2 and CC7, that originate from two genetically distinct lineages and that differ in their Symbiodinium specificity. However, little is known about their other microbial associations. Here, we examined and compared the taxonomic composition of the bacterial assemblages of these two symbiotic Exaiptasia strains, both of which have been cultured in the laboratory long-term under identical conditions. We found distinct bacterial microbiota for each strain, indicating the presence of host-specific microbial consortia. Putative differences in the bacterial functional profiles (i.e., enrichment and depletion of various metabolic processes) based on taxonomic inference were also detected, further suggesting functional differences of the microbiomes associated with these lineages. Our study contributes to the current knowledge of the Exaiptasia holobiont by comparing the bacterial diversity of two commonly used strains as models for coral research.
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    Association of coral algal symbionts with a diverse viral community responsive to heat shock

    Brüwer, Jan D.; Agrawal, Shobhit; Liew, Yi Jin; Aranda, Manuel; Voolstra, Christian R. (BMC Microbiology, Springer Nature, 2017-08-17) [Article]
    Stony corals provide the structural foundation of coral reef ecosystems and are termed holobionts given they engage in symbioses, in particular with photosynthetic dinoflagellates of the genus Symbiodinium. Besides Symbiodinium, corals also engage with bacteria affecting metabolism, immunity, and resilience of the coral holobiont, but the role of associated viruses is largely unknown. In this regard, the increase of studies using RNA sequencing (RNA-Seq) to assess gene expression provides an opportunity to elucidate viral signatures encompassed within the data via careful delineation of sequence reads and their source of origin.Here, we re-analyzed an RNA-Seq dataset from a cultured coral symbiont (Symbiodinium microadriaticum, Clade A1) across four experimental treatments (control, cold shock, heat shock, dark shock) to characterize associated viral diversity, abundance, and gene expression. Our approach comprised the filtering and removal of host sequence reads, subsequent phylogenetic assignment of sequence reads of putative viral origin, and the assembly and analysis of differentially expressed viral genes. About 15.46% (123 million) of all sequence reads were non-host-related, of which <1% could be classified as archaea, bacteria, or virus. Of these, 18.78% were annotated as virus and comprised a diverse community consistent across experimental treatments. Further, non-host related sequence reads assembled into 56,064 contigs, including 4856 contigs of putative viral origin that featured 43 differentially expressed genes during heat shock. The differentially expressed genes included viral kinases, ubiquitin, and ankyrin repeat proteins (amongst others), which are suggested to help the virus proliferate and inhibit the algal host's antiviral response.Our results suggest that a diverse viral community is associated with coral algal endosymbionts of the genus Symbiodinium, which prompts further research on their ecological role in coral health and resilience.
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    Data from: Using a butterflyfish genome as a general tool for RAD-Seq studies in specialized reef fish

    DiBattista, Joseph; Saenz Agudelo, Pablo; Piatek, Marek J.; Wang, Xin; Aranda, Manuel; Berumen, Michael L. (Dryad Digital Repository, 2017) [Dataset]
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    Recent expansion of heat-activated retrotransposons in the coral symbiont Symbiodinium microadriaticum

    Chen, Jit Ern; Cui, Guoxin; Wang, Xin; Liew, Yi Jin; Aranda, Manuel (The ISME Journal, Springer Nature, 2017-10-20) [Article]
    Rising sea surface temperature is the main cause of global coral reef decline. Abnormally high temperatures trigger the breakdown of the symbiotic association between corals and their photosynthetic symbionts in the genus Symbiodinium. Higher genetic variation resulting from shorter generation times has previously been proposed to provide increased adaptability to Symbiodinium compared to the host. Retrotransposition is a significant source of genetic variation in eukaryotes and some transposable elements are specifically expressed under adverse environmental conditions. We present transcriptomic and phylogenetic evidence for the existence of heat stress-activated Ty1-copia-type LTR retrotransposons in the coral symbiont Symbiodinium microadriaticum. Genome-wide analyses of emergence patterns of these elements further indicate recent expansion events in the genome of S. microadriaticum. Our findings suggest that acute temperature increases can activate specific retrotransposons in the Symbiodinium genome with potential impacts on the rate of retrotransposition and the generation of genetic variation under heat stress.The ISME Journal advance online publication, 20 October 2017; doi:10.1038/ismej.2017.179.
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    Genome based analyses of six hexacorallian species reject the “naked coral” hypothesis

    Wang, Xin; Drillon, Guénola; Ryu, Taewoo; Voolstra, Christian R.; Aranda, Manuel (Genome Biology and Evolution, Oxford University Press (OUP), 2017-09-23) [Article]
    Scleractinian corals are the foundation species of the coral-reef ecosystem. Their calcium carbonate skeletons form extensive structures that are home to millions of species, making coral reefs one of the most diverse ecosystems of our planet. However, our understanding of how reef-building corals have evolved the ability to calcify and become the ecosystem builders they are today is hampered by uncertain relationships within their subclass Hexacorallia. Corallimorpharians have been proposed to originate from a complex scleractinian ancestor that lost the ability to calcify in response to increasing ocean acidification, suggesting the possibility for corals to lose and gain the ability to calcify in response to increasing ocean acidification. Here we employed a phylogenomic approach using whole-genome data from six hexacorallian species to resolve the evolutionary relationship between reef-building corals and their non-calcifying relatives. Phylogenetic analysis based on 1,421 single-copy orthologs, as well as gene presence/absence and synteny information, converged on the same topologies, showing strong support for scleractinian monophyly and a corallimorpharian sister clade. Our broad phylogenomic approach using sequence-based and sequence-independent analyses provides unambiguous evidence for the monophyly of scleractinian corals and the rejection of corallimorpharians as descendants of a complex coral ancestor.
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    DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia

    Li, Yong; Liew, Yi Jin; Cui, Guoxin; Cziesielski, Maha Joana; Zahran, Noura Ibrahim Omar; Michell, Craig T; Voolstra, Christian R.; Aranda, Manuel (Cold Spring Harbor Laboratory, 2017-11-03) [Preprint]
    The symbiotic relationship between cnidarians and dinoflagellates is the cornerstone of coral reef ecosystems. Although research is focusing on the molecular mechanisms underlying this symbiosis, the role of epigenetic mechanisms, which have been implicated in transcriptional regulation and acclimation to environmental change, is unknown. To assess the role of DNA methylation in the cnidarian-dinoflagellate symbiosis, we analyzed genome-wide CpG methylation, histone associations, and transcriptomic states of symbiotic and aposymbiotic anemones in the model system Aiptasia. We find methylated genes are marked by histone H3K36me3 and show significant reduction of spurious transcription and transcriptional noise, revealing a role of DNA methylation in the maintenance of transcriptional homeostasis. Changes in DNA methylation and expression show enrichment for symbiosis-related processes such as immunity, apoptosis, phagocytosis recognition and phagosome formation, and unveil intricate interactions between the underlying pathways. Our results demonstrate that DNA methylation provides an epigenetic mechanism of transcriptional homeostasis during symbiosis.
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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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    Using a butterflyfish genome as a general tool for RAD-Seq studies in specialized reef fish

    DiBattista, Joseph; Saenz Agudelo, Pablo; Piatek, Marek J.; Wang, Xin; Aranda, Manuel; Berumen, Michael L. (Molecular Ecology Resources, Wiley, 2017-04-06) [Article]
    Data from a large-scale restriction site associated DNA (RAD-Seq) study of nine butterflyfish species in the Red Sea and Arabian Sea provided a means to test the utility of a recently published draft genome (Chaetodon austriacus) and assess apparent bias in this method of isolating nuclear loci. We here processed double-digest restriction-site (ddRAD) associated DNA sequencing data to identify single nucleotide polymorphism (SNP) markers and their associated function with and without our reference genome to see if it improves the quality of RAD-Seq markers. Our analyses indicate (1) a modest gap between the number of non-annotated versus annotated SNPs across all species, (2) an advantage of using genomic resources for closely related but not distantly related butterflyfish species based on the ability to assign putative gene function to SNPs, and (3) an enrichment of genes among sister butterflyfish taxa related to calcium transmembrane transport and binding. The latter result highlights the potential for this approach to reveal insights into adaptive mechanisms in populations inhabiting challenging coral reef environments such as the Red Sea, Arabian Sea, and Arabian Gulf with further study.
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    Draft genomes of the corallimorpharians Amplexidiscus fenestrafer and Discosoma sp

    Wang, Xin; Liew, Yi Jin; Li, Yong; Zoccola, Didier; Tambutte, Sylvie; Aranda, Manuel (Molecular Ecology Resources, Wiley, 2017-06-27) [Article]
    Corallimorpharia are the closest non-calcifying relatives of reef-building corals. Aside from their popularity among aquarium hobbyists, their evolutionary position between the Actiniaria (sea anemones) and the Scleractinia (hard corals) makes them ideal candidates for comparative studies aiming at understanding the evolution of hexacorallian orders in general and reef-building corals in particular. Here we have sequenced and assembled two draft genomes for the Corallimorpharia species Amplexidiscus fenestrafer and Discosoma sp.. The draft genomes encompass 370 Mbp and 445 Mbp respectively and encode for 21,372 and 23,199 genes. To facilitate future studies using these resources, we provide annotations for the predicted gene models-not only at gene level, by annotating gene models with the function of the best-matching homolog, and GO terms when available; but also at protein domain level, where gene function can be better verified through the conservation of the sequence and order of protein domains. Further, we provide an online platform (http://corallimorpharia.reefgenomics.org), which includes a BLAST interface as well as a genome browser to facilitate the use of these resources. We believe that these two genomes are important resources for future studies on hexacorallian systematics and the evolutionary basis of their specific traits such as the symbiotic relationship with dinoflagellates of the genus Symbiodinium or the evolution of calcification in reef-building corals. This article is protected by copyright. All rights reserved.
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