Host nutrient sensing is mediated by mTOR signaling in cnidarian-dinoflagellate symbiosis

Voss, Philipp A.; Gornik, Sebastian G.; Jacobovitz, Marie R.; Rupp, Sebastian; Dörr, Melanie; Maegele, Ira; Guse, Annika

doi:10.1016/j.cub.2023.07.038

Cited by 3 publications

(6 citation statements)

References 105 publications

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“…Nutrient sensing at the lysosome can occur via the mechanistic target of rapamycin (mTOR) complex 1 (mTORC1), part of the highly conserved mTOR signaling pathway, which is active in symbiosis (85,157). In Aiptasia, mTOR signaling is activated upon symbiosis establishment, where mTOR localizes to symbiosomes in adults and larvae.…”

Section: Nutrient Sensing and Host Cell Proliferation And Growthmentioning

confidence: 99%

“…In Aiptasia, mTOR signaling is activated upon symbiosis establishment, where mTOR localizes to symbiosomes in adults and larvae. When mTOR signaling is inhibited, the LAMP1 niche is not established and symbiosis breaks down-a mechanism that is conserved in the coral A. tenuis (157). Symbiosis positively influences host cell proliferation in both endodermal and ectodermal tissues in Aiptasia larvae and adults, depending on symbiont strain and host nutritional status (47,147,157).…”

Section: Nutrient Sensing and Host Cell Proliferation And Growthmentioning

confidence: 99%

“…When mTOR signaling is inhibited, the LAMP1 niche is not established and symbiosis breaks down-a mechanism that is conserved in the coral A. tenuis (157). Symbiosis positively influences host cell proliferation in both endodermal and ectodermal tissues in Aiptasia larvae and adults, depending on symbiont strain and host nutritional status (47,147,157). Taken together, cellular and organismal responses to nutrient fluxes, including by mTOR signaling, are key for symbiont-derived nutrient integration in symbiotic cnidarians.…”

Section: Nutrient Sensing and Host Cell Proliferation And Growthmentioning

confidence: 99%

“…The importance of nutrient exchange for coral-dinoflagellate symbiosis is evident when examining the effects of disruptions to this process. Several studies have demonstrated dysbiosis and bleaching by interfering with these essential nutrient exchange processes (122,133,148,157,164,168). To highlight just one example utilizing NanoSIMS, as the metabolic energy demand of the coral S. pistillata host increases during heat stress, amino acids were catabolized as a compensatory mechanism, demonstrating that changes in nutrient cycling induced by heat stress are a primary driver of the breakdown of coraldinoflagellate symbiosis (121).…”

Section: 36mentioning

confidence: 99%

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Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach

Jacobovitz,

Hambleton,

Guse

2023

Annu. Rev. Genet.

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Symbiotic interactions occur in all domains of life, providing organisms with resources to adapt to new habitats. A prime example is the endosymbiosis between corals and photosynthetic dinoflagellates. Eukaryotic dinoflagellate symbionts reside inside coral cells and transfer essential nutrients to their hosts, driving the productivity of the most biodiverse marine ecosystem. Recent advances in molecular and genomic characterization have revealed symbiosis-specific genes and mechanisms shared among symbiotic cnidarians. In this review, we focus on the cellular and molecular processes that underpin the interaction between symbiont and host. We discuss symbiont acquisition via phagocytosis, modulation of host innate immunity, symbiont integration into host cell metabolism, and nutrient exchange as a fundamental aspect of stable symbiotic associations. We emphasize the importance of using model systems to dissect the cellular complexity of endosymbiosis, which ultimately serves as the basis for understanding its ecology and capacity to adapt in the face of climate change. Expected final online publication date for the Annual Review of Genetics, Volume 57 is November 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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Section: Nutrient Sensing and Host Cell Proliferation And Growthmentioning

confidence: 99%

Section: Nutrient Sensing and Host Cell Proliferation And Growthmentioning

confidence: 99%

Section: Nutrient Sensing and Host Cell Proliferation And Growthmentioning

confidence: 99%

Section: 36mentioning

confidence: 99%

See 2 more Smart Citations

Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach

Jacobovitz,

Hambleton,

Guse

2023

Annu. Rev. Genet.

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“…In Hydra , inhibition of TOR signalling by Rapamycin leads to increased autophagy but the role of TOR in body size and cell proliferation remains unexplored ( Chera et al, 2009 ). Signalling via TOR kinase has recently been shown to also regulate nutrient sensing during the cnidarian-dinoflagellate symbiosis in Exaiptasia diaphana (Aiptasia; Voss et al, 2023 ). In Nematostella primary polyps, TOR signalling is essential for the induction of tentacle growth and global cell proliferation after the initiation of feeding ( Ikmi et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

The cellular basis of feeding-dependent body size plasticity in sea anemones

Garschall,

Pascual-Carreras,

García-Pascual

et al. 2024

Development

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Many animals share a lifelong capacity to adapt their growth rates and body sizes to changing environmental food supplies. However, the cellular and molecular basis underlying this plasticity remains only poorly understood. We therefore studied how the sea anemones Nematostella vectensis and Aiptasia (Exaiptasia pallida) respond to feeding and starvation. Combining quantifications of body size and cell numbers with mathematical modelling, we observed that growth and shrinkage rates in Nematostella are exponential, stereotypic and accompanied by dramatic changes in cell numbers. Notably, shrinkage rates, but not growth rates, are independent of body size. In the facultatively symbiotic Aiptasia, we show that growth and cell proliferation rates are dependent on the symbiotic state. On a cellular level, we found that >7% of all cells in Nematostella juveniles reversibly shift between S/G2/M and G1/G0 cell cycle phases when fed or starved, respectively. Furthermore, we demonstrate that polyp growth and cell proliferation are dependent on TOR signalling during feeding. Altogether, we provide a benchmark and resource for further investigating the nutritional regulation of body plasticity on multiple scales using the genetic toolkit available for Nematostella.

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Cholinergic regulation of sleep in the upside-down jellyfishCassiopea

Abrams,

Ohdera,

Francis

et al. 2024

Preprint

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Perhaps nothing is stronger evidence of the importance of sleep than its conservation across animals, but the extent of its regulatory conservation is unknown. The upside-down jellyfish Cassiopea xamachana sleeps, and this behavior is controlled by radially-spaced marginal ganglia. After defining a sleep-wake threshold, we compared gene expression profiles of ganglia from animals sleep-deprived for two nights and found differential expression in many sleep-related genes including GABAergic, melatonergic, and cholinergic receptors. We focused on a nicotinic acetylcholine receptor alpha subunit-like (Chrnal-E), based on its differential expression, and selected animals for a second round of RNAseq that included both light-based and mechanically-based sleep-deprivation. Combining datasets revealed a short list of differentially expressed genes, of which chrnal-E is the most recognizable and well-supported, so we investigated its potential role in sleep regulation. First, we found that chemical cholinergic neuromodulators positively regulate pacemaker activity. Then, we showed by in situ hybridization that chrnal-E is expressed primarily within the ganglia, and that the area of expression expands after sleep deprivation. Next, we developed RNAi for use in Cassiopea and determined that Chrnal-E promotes wakefulness. Finally, we sampled circadian timepoints in the field and found in control conditions, chrnal-E has lowest expression late at night, but in sleep deprived animals, chrnal-E peaks at this time, supporting a link to wakefulness. Our finding that Cassiopea sleep is regulated by the cholinergic system underscores that mechanisms of sleep conservation are deeply conserved in animal evolution.

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Host nutrient sensing is mediated by mTOR signaling in cnidarian-dinoflagellate symbiosis

Cited by 3 publications

References 105 publications

Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach

Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach

The cellular basis of feeding-dependent body size plasticity in sea anemones

Cholinergic regulation of sleep in the upside-down jellyfishCassiopea

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