Nutrient-dependent mTORC1 signaling in coral-algal symbiosis

Abstract

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 symbiosis with intracellular photosynthetic dinoflagellates (family Symbiodiniaceae (LaJeunesse et al., 2018)). Symbionts reside in 'symbiosomes' 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 lifestyle. Here we use the symbiosis model Exaiptasia pallida (hereafter Aiptasia) to address this. Aiptasia larvae, 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 symbiosis establishment results in downregulation of various catabolic pathways, including autophagy in host cells. This metabolic switch is likely triggered by the highly-conserved mTORC1 (mechanistic target of rapamycin complex 1) signaling cascade, shown to integrate lysosomal nutrient abundance with animal development (Perera and Zoncu, 2016). Specifically, symbiosomes are LAMP1-positive and recruit mTORC1 kinase. In symbiotic anemones, mTORC1 signaling is elevated when compared to non-symbiotic animals, resembling a feeding response. Moreover, symbiosis establishment enhances lipid content and cell proliferation in Aiptasia larvae. Challenging the prevailing belief that symbiosomes are early arrested phagosomes (Mohamed et al., 2016), we propose a model in which symbiosomes functionally resemble lysosomes as core nutrient sensing and signaling hubs that have co-opted the evolutionary ancient mTORC1 pathway to promote growth in endosymbiotic cnidarians.

Dinoflagellate symbionts escape vomocytosis by host cell immune suppression

“…2a, Fig. S2b) (Voss et al, 2019). In contrast, M. gaditanacontaining cells are basically indistinguishable at the transcriptional level from aposymbiotic cells ( Fig.…”

“…RNA sequencing data from Voss, et al (2019) results was restricted to pathways involved in innate immunity as found in KEGG (Kanehisa and Goto, 2000), using the R! package "ComplexHeatmap" (Gu et al, 2016) in KNIME (Berthold et al, 2007).…”

“…We compared M. gaditana-containing endodermal cells and aposymbiotic endodermal cells to endodermal cells containing symbionts and aposymbiotic cells from symbiotic larvae, as well as cells from aposymbiotic larvae ( Fig. S2a) (Voss et al, 2019). Using this cell-type specific approach, we found that only cells containing symbionts are clearly distinct in their overall gene expression when compared to all other cell types ( Fig.…”

“…1d), using our recently developed cell-specific RNAseq approach (Fig. S2a) (Voss et al, 2019). We infected Aiptasia larvae with M. gaditana for 24-48 h, dissociated infected larvae, and sequenced groups of 8-12 endodermal cells that contained M. gaditana cells and aposymbiotic cells from M. gaditana-infected larvae.…”

“…PBS-Triton and one wash in PBS. Larvae were then permeabilised in PBS-Triton for 1.5 h at RT, followed by blocking in 5% normal goat serum and 1% BSA in PBS-Triton for 1 h. Primary antibody (rabbit-α-LAMP1) (Voss et al, 2019) was diluted 1:100 in blocking buffer and incubated overnight at 4°C. After three washes in PBS-Triton, the secondary antibody (goat-α-rabbit AlexaFluor 488, #ab150089, abcam) was diluted 1:500 in blocking buffer and incubated for 1.5 h at RT.…”