Endosymbiosis drives transcriptomic adjustements and genomic adapatations in cnidarians

To decipher inter-partner signaling within the cnidarian-dinoflagellate endosymbiosis, we developed genomic resources (cDNA library and microarrays) for the symbiotic sea anemone Anemonia viridis. Differential gene expression was quantified during thermal stress, with and without UV radiation, between symbiotic vs aposymbiotic specimens and gastroderm vs epidermis tissues. During stress time-course experiments, each stress showed a specific gene expression profile with very little overlap. We show that the major response to thermal stress is rapid (24 hours) but returns to the baseline levels after 2 days. UVR alone has little effect but potentiates thermal stress, as expression of a second set of genes becomes differentially expressed at day 5. Analysis of genes differentially expressed between symbiotic vs bleached and symbiotic vs stressed specimens defined a restricted subset of genes (Kern). Tissue specific expression mapping of Kern genes showed that many were specifically enhanced in the symbiotic cells (gastroderm). Altogether, these data define the Kern genes as major molecular components of the symbiotic interaction. Functional annotations highlighted several pathways including collagen fibrillogenesis, vesicular trafficking, lipid metabolism, calcium signaling, inorganic carbon transfer and cell death, that were modified by stress. Phylogenomic investigations of several Kern genes (calumenin, NPC2, SYM32, dermatopontin, and Rhbg) demonstrate that these issued from cnidarian specific duplication events, with the Kern member being preferentially expressed in the gastroderm and specifically responding to stress. Such host specific genes subfunctionalizations suggest both genomic and transcriptomic adaptations driven by the physiological constraints of endosymbiosis

Evolutionary origin of synapses and neurons – Bridging the gap

The evolutionary origin of synapses and neurons is an enigmatic subject that inspires much debate. Non-bilaterian metazoans, both with and without neurons and their closest relatives already contain many components of the molecular toolkits for synapse functions. The origin of these components and their assembly into ancient synaptic signaling machineries are particularly important in light of recent findings on the phylogeny of non-bilaterian metazoans. The evolution of synapses and neurons are often discussed only from a metazoan perspective leaving a considerable gap in our understanding. By taking an integrative approach we highlight the need to consider different, but extremely relevant phyla and to include the closest unicellular relatives of metazoans, the ichthyosporeans, filastereans and choanoflagellates, to fully understand the evolutionary origin of synapses and neurons. This approach allows for a detailed understanding of when and how the first pre- and postsynaptic signaling machineries evolved

Evolutionary origin of synapses and neurons - Bridging the gap

The evolutionary origin of synapses and neurons is an enigmatic subject that inspires much debate. Non-bilaterian metazoans, both with and without neurons and their closest relatives already contain many components of the molecular toolkits for synapse functions. The origin of these components and their assembly into ancient synaptic signaling machineries are particularly important in light of recent findings on the phylogeny of non-bilaterian metazoans. The evolution of synapses and neurons are often discussed only from a metazoan perspective leaving a considerable gap in our understanding. By taking an integrative approach we highlight the need to consider different, but extremely relevant phyla and to include the closest unicellular relatives of metazoans, the ichthyosporeans, filastereans and choanoflagellates, to fully understand the evolutionary origin of synapses and neurons. This approach allows for a detailed understanding of when and how the first pre- and postsynaptic signaling machineries evolved

Adaptations to Endosymbiosis in a Cnidarian-Dinoflagellate Association: Differential Gene Expression and Specific Gene Duplications

Trophic endosymbiosis between anthozoans and photosynthetic dinoflagellates forms the key foundation of reef ecosystems. Dysfunction and collapse of symbiosis lead to bleaching (symbiont expulsion), which is responsible for the severe worldwide decline of coral reefs. Molecular signals are central to the stability of this partnership and are therefore closely related to coral health. To decipher inter-partner signaling, we developed genomic resources (cDNA library and microarrays) from the symbiotic sea anemone Anemonia viridis. Here we describe differential expression between symbiotic (also called zooxanthellate anemones) or aposymbiotic (also called bleached) A. viridis specimens, using microarray hybridizations and qPCR experiments. We mapped, for the first time, transcript abundance separately in the epidermal cell layer and the gastrodermal cells that host photosynthetic symbionts. Transcriptomic profiles showed large inter-individual variability, indicating that aposymbiosis could be induced by different pathways. We defined a restricted subset of 39 common genes that are characteristic of the symbiotic or aposymbiotic states. We demonstrated that transcription of many genes belonging to this set is specifically enhanced in the symbiotic cells (gastroderm). A model is proposed where the aposymbiotic and therefore heterotrophic state triggers vesicular trafficking, whereas the symbiotic and therefore autotrophic state favors metabolic exchanges between host and symbiont. Several genetic pathways were investigated in more detail: i) a key vitamin K–dependant process involved in the dinoflagellate-cnidarian recognition; ii) two cnidarian tissue-specific carbonic anhydrases involved in the carbon transfer from the environment to the intracellular symbionts; iii) host collagen synthesis, mostly supported by the symbiotic tissue. Further, we identified specific gene duplications and showed that the cnidarian-specific isoform was also up-regulated both in the symbiotic state and in the gastroderm. Our results thus offer new insight into the inter-partner signaling required for the physiological mechanisms of the symbiosis that is crucial for coral health

Endosymbiosis drives transcriptomic adjustements and genomic adapatations in cnidarians

To decipher inter-partner signaling within the cnidarian-dinoflagellate endosymbiosis, we developed genomic resources (cDNA library and microarrays) for the symbiotic sea anemone Anemonia viridis. Differential gene expression was quantified during thermal stress, with and without UV radiation, between symbiotic vs aposymbiotic specimens and gastroderm vs epidermis tissues. During stress time-course experiments, each stress showed a specific gene expression profile with very little overlap. We show that the major response to thermal stress is rapid (24 hours) but returns to the baseline levels after 2 days. UVR alone has little effect but potentiates thermal stress, as expression of a second set of genes becomes differentially expressed at day 5. Analysis of genes differentially expressed between symbiotic vs bleached and symbiotic vs stressed specimens defined a restricted subset of genes (Kern). Tissue specific expression mapping of Kern genes showed that many were specifically enhanced in the symbiotic cells (gastroderm). Altogether, these data define the Kern genes as major molecular components of the symbiotic interaction. Functional annotations highlighted several pathways including collagen fibrillogenesis, vesicular trafficking, lipid metabolism, calcium signaling, inorganic carbon transfer and cell death, that were modified by stress. Phylogenomic investigations of several Kern genes (calumenin, NPC2, SYM32, dermatopontin, and Rhbg) demonstrate that these issued from cnidarian specific duplication events, with the Kern member being preferentially expressed in the gastroderm and specifically responding to stress. Such host specific genes subfunctionalizations suggest both genomic and transcriptomic adaptations driven by the physiological constraints of endosymbiosis

Data from: Are Niemann-Pick type C proteins key players in cnidarian-dinoflagellate endosymbioses?

The symbiotic interaction between cnidarians, such as corals and sea anemones, and the unicellular algae Symbiodinium is regulated by yet poorly understood cellular mechanisms, despite the ecological importance of coral reefs. These mechanisms, including host-symbiont recognition and metabolic exchange, control symbiosis stability under normal conditions, but also lead to symbiosis breakdown (bleaching) during stress. This study describes the repertoire of the sterol-trafficking proteins Niemann-Pick type C (NPC1 and NPC2) in the symbiotic sea anemone Anemonia viridis. We found one NPC1 gene instead of two in vertebrates. While only one NPC2 gene is present in most metazoans, this gene has been duplicated in cnidarians and we detected four NPC2 genes in A. viridis. However, only one gene (AvNPC2-d) was upregulated in symbiotic sea anemones and displayed higher expression in the gastrodermis (symbiont-containing tissue) than in the epidermis. We performed immunolabeling experiments on tentacle cross sections and demonstrated that the AvNPC2-d protein was closely associated with symbiosomes. In addition, AvNPC1 and AvNPC2-d gene expression was strongly downregulated during stress, especially at the onset of symbiosis breakdown. These data suggest that AvNPC2-d is involved in both the stability and dysfunction of cnidarian-dinoflagellate symbioses

An alternative and effective method for extracting skeletal organic matrix adapted to the red coral Corallium rubrum

International audienceSkeleton formation in corals is a biologically controlled process in which an extracellular organic matrix (OM) is entrapped inside the calcified structure. The analysis of OM requires a time-consuming and tedious extraction that includes grinding, demineralization, multiple rinsing and concentration steps. Here we present an alternative and straightforward method for the red coral Corallium rubrum that requires little equipment and saving steps. The entire skeleton is directly demineralized to produce a tractable material called ghost, which is further rinsed and melted at 80 °C in water. The comparative analysis of the standard and alternative methods by electrophoresis, Western blot, and FTIR of C. rubrum OM, shows that the "alternative OM" is of higher quality. Advantages and limitations of both methods are discussed