Extensive Differences in Gene Expression Between Symbiotic and Aposymbiotic Cnidarians

Abstract

Coral reefs provide habitats for a disproportionate number of marine species relative to the small area of the oceans that they occupy. The mutualism between the cnidarian animal hosts and their intracellular dinoflagellate symbionts provides the nutritional foundation for coral growth and formation of reef structures, because algal photosynthesis can provide >90% of the total energy of the host. Disruption of this symbiosis (“coral bleaching”) is occurring on a large scale due primarily to anthropogenic factors and poses a major threat to the future of coral reefs. Despite the importance of this symbiosis, the cellular mechanisms involved in its establishment, maintenance, and breakdown remain largely unknown. We report our continued development of genomic tools to study these mechanisms in Aiptasia, a small sea anemone with great promise as a model system for studies of cnidarian–dinoflagellate symbiosis. Specifically, we have generated de novo assemblies of the transcriptomes of both a clonal line of symbiotic anemones and their endogenous dinoflagellate symbionts. We then compared transcript abundances in animals with and without dinoflagellates. This analysis identified >900 differentially expressed genes and allowed us to generate testable hypotheses about the cellular functions affected by symbiosis establishment. The differentially regulated transcripts include >60 encoding proteins that may play roles in transporting various nutrients between the symbiotic partners; many more encoding proteins functioning in several metabolic pathways, providing clues regarding how the transported nutrients may be used by the partners; and several encoding proteins that may be involved in host recognition and tolerance of the dinoflagellate.

The genome of Aiptasia , a sea anemone model for coral symbiosis

“…The Aiptasia genome sequence should help to elucidate these matters, as the following examples illustrate. First, BLASTP (protein basic local alignment search tool) searches of the gene models confirm previous transcriptomic evidence (19) that anthozoans, like other animals, lack the ability to synthesize 12 of the 20 common amino acids from central-pathway intermediates (SI Appendix, Table S8). The missing enzymes include two that are essential for the synthesis of the sulfur-containing amino acids, but the genome also confirms that Aiptasia, like other animals including N. vectensis (SI Appendix, Table S8) and several corals (9), contains a gene for a cystathionine-β-synthase, so that it should be able to synthesize cysteine from methionine (19).…”

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

“…These shifts are likely due to the ongoing energetic costs associated with maintaining homeostasis under elevated temperature, such as modifications to the structure of cell membranes, which in turn necessitate the generation of energy from alternate pathway modes (as discussed above) (Coles and Jokiel, 1977;Clark and Jensen, 1982), such as via gluconeogenesis and beta-oxidation, in the breakdown of proteins and lipids (Lehnert et al, 2014).…”

Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasiasp.) for symbiosis investigations

“…aposymbiotic combines temperature stress (heat or cold shock) followed by dark treatment and/or chemical inhibition of photosynthesis with 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) (e.g. Belda-Baillie et al, 2002;Lehnert et al, 2014;Xiang et al, 2013). This is a slow, laborious process that often requires months of preparation (Starzak et al, 2014;Xiang et al, 2013), and may not result in the full eradication of in hospite endosymbionts (Belda-Baillie et al, 2002;Schoenberg and Trench, 1980;Wang and Douglas, 1998).…”