Röthig, Till; Martins Da Costa, Ruben; Simona, Fabia; Baumgarten, Sebastian; Torres, Ana F.; Radhakrishnan, Anand; Aranda, Manuel; Voolstra, Christian R.(Frontiers in Marine Science, Frontiers Media SA, 2016-11-18)[Article]
Coral reefs are in decline. The basic functional unit of coral reefs is the coral metaorganism or holobiont consisting of the cnidarian host animal, symbiotic algae of the genus Symbiodinium, and a specific consortium of bacteria (among others), but research is slow due to the difficulty of working with corals. Aiptasia has proven to be a tractable model system to elucidate the intricacies of cnidarian-dinoflagellate symbioses, but characterization of the associated bacterial microbiome is required to provide a complete and integrated understanding of holobiont function. In this work, we characterize and analyze the microbiome of aposymbiotic and symbiotic Aiptasia and show that bacterial associates are distinct in both conditions. We further show that key microbial associates can be cultured without their cnidarian host. Our results suggest that bacteria play an important role in the symbiosis of Aiptasia with Symbiodinium, a finding that underlines the power of the Aiptasia model system where cnidarian hosts can be analyzed in aposymbiotic and symbiotic states. The characterization of the native microbiome and the ability to retrieve culturable isolates contributes to the resources available for the Aiptasia model system. This provides an opportunity to comparatively analyze cnidarian metaorganisms as collective functional holobionts and as separated member species. We hope that this will accelerate research into understanding the intricacies of coral biology, which is urgently needed to develop strategies to mitigate the effects of environmental change.
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.
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.
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.
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.
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.
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.
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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