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

Abstract

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.

Evolution of TNF-induced apoptosis reveals 550 My of functional conservation

“…Although previous work has investigated the downstream effectors of apoptosis such as caspases (43) and Bcl-2 family members (42), this is the first examination, to our knowledge, of the upstream ligands and receptors involved with initiating apoptosis in coral. Recently published transcriptomic studies of corals exposed to various environmental stressors have implicated members of the TNFSF/TNFRSF, as well as downstream proteins involved with apoptosis, supporting the ecological relevance of the TNF pathway in coral (45)(46)(47)(48)(49).…”

Cell Biology of Cnidarian-Dinoflagellate Symbiosis

“…Weis and Reynolds (400) subsequently used an anti-human CA immunoprobe and semiquantitative PCR to quantify increased amounts of the enzyme and its transcript, respectively, in the temperate sea anemone Anthopleura elegantissima when symbiotic versus aposymbiotic, and in the process they provided the first direct evidence of a host gene whose expression is influenced by its symbiotic dinoflagellates; these authors also, for the first time, reported a full-length CA cDNA sequence from a symbiotic cnidarian. Most recently, by employing a genomic approach, Ganot et al (122) have confirmed that CA expression is under the control of the symbiotic state.…”

“…Two of the most highly upregulated genes in symbiotic anemones encode sym32, a protein described first in Anthopleura elegantissima (311,326,399) and more recently in Anemonia viridis (122), and calumenin (122). Ganot and coworkers (122) have developed a testable model for the role that these two proteins play in recognition and tolerance of symbionts.…”

Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis

“…Organic acids and pathway intermediates play essential roles in central metabolic pathways, including the TCA cycle, glycolysis, oxidative phosphorylation, the pentose phosphate pathway and gluconeogenesis (Livingstone, 1991;Ganot et al, 2011;Butterfield et al, 2013). They also have important functions in the production of co-enzymes and antioxidants, and as signalling molecules (Krüger et al, 2011).…”