Nutrient-dependent mTORC1 signaling in coral-algal symbiosis

To coordinate development and growth with nutrient availability, animals must sense nutrients and acquire food from the environment once energy is depleted. A notable exception are reef-building corals that form a stable symbiosiswith intracellular photosynthetic dinoflagellates (family Symbiodiniaceae (LaJeunesse et al., 2018)). Symbionts reside in 9symbiosomes9 and transfer key nutrients to support nutrition and growth of their coral host in nutrient-poor environments (Muscatine, 1990; Yellowlees et al., 2008). To date, it is unclear how symbiont-provided nutrients are sensed to adapt host physiology to this endosymbiotic life-style. Here we use the symbiosismodel Exaiptasia pallida(hereafter Aiptasia) to address this. Aiptasialarvae, similar to their coral relatives, are naturally non-symbiotic and phagocytose symbionts anew each generation into their endodermal cells (Bucher et al., 2016; Grawunder et al., 2015; Hambleton et al., 2014). Using cell-specific transcriptomics, we find that symbiosisestablishment results in downregulation of various catabolic pathways, including autophagy in host cells. This metabolic switch is likely triggered by the highly-conserved mTORC1( mechanistic targetof rapamycincomplex 1) signaling cascade, shown to integrate lysosomal nutrient abundance with animal development (Perera and Zoncu, 2016). Specifically, symbiosomesare LAMP1-positive and recruit mTORC1kinase. In symbiotic anemones, mTORC1signaling is elevated when compared to non-symbiotic animals, resembling a feeding response. Moreover, symbiosisestablishment enhances lipid content and cell proliferation in Aiptasialarvae. Challenging the prevailing belief that symbiosomesare early arrested phagosomes(Mohamed et al., 2016), we propose a model in which symbiosomesfunctionally resemble lysosomes as core nutrient sensingand signaling hubs that have co-opted the evolutionary ancient mTORC1pathway to promote growth in endosymbiotic cnidarians.