Dual RNA-sequencing analyses of a coral and its native symbiont during the establishment of symbiosis

Abstract

Despite the ecological significance of the mutualistic relationship between Symbiodiniaceae and reef‐building corals, the molecular interactions during establishment of this relationship are not well understood. This is particularly true of the transcriptional changes that occur in the symbiont. In the current study, a dual RNA‐sequencing approach was used to better understand transcriptional changes on both sides of the coral–symbiont interaction during the colonization of Acropora tenuis by a compatible Symbiodiniaceae strain (Cladocopium goreaui; ITS2 type C1). Comparison of transcript levels of the in hospite symbiont 3, 12, 48 and 72 hr after exposure to those of the same strain in culture revealed that extensive and generalized down‐regulation of symbiont gene expression occurred during the infection process. Included in this “symbiosis‐derived transcriptional repression” were a range of stress response and immune‐related genes. In contrast, a suite of symbiont genes implicated in metabolism was upregulated in the symbiotic state. The coral data support the hypothesis that immune‐suppression and arrest of phagosome maturation play important roles during the establishment of compatible symbioses, and additionally imply the involvement of some SCRiP family members in the colonization process. Consistent with previous ecological studies, the transcriptomic data suggest that active translocation of metabolites to the host may begin early in the colonization process, and thus that the mutualistic relationship can be established at the larval stage. This dual RNA‐sequencing study provides insights into the transcriptomic remodelling that occurs in C. goreaui during transition to a symbiotic lifestyle and the novel coral genes implicated in symbiosis.