A carbon-nitrogen negative feedback loop underlies the repeated evolution of cnidarian–Symbiodiniaceae symbioses

Abstract

Symbiotic associations with Symbiodiniaceae have evolved independently across a diverse range of cnidarian taxa including reef-building corals, sea anemones, and jellyfish, yet the molecular mechanisms underlying their regulation and repeated evolution are still elusive. Here, we show that despite their independent evolution, cnidarian hosts use the same carbon-nitrogen negative feedback loop to control symbiont proliferation. Symbiont-derived photosynthates are used to assimilate nitrogenous waste via glutamine synthetase–glutamate synthase-mediated amino acid biosynthesis in a carbon-dependent manner, which regulates the availability of nitrogen to the symbionts. Using nutrient supplementation experiments, we show that the provision of additional carbohydrates significantly reduces symbiont density while ammonium promotes symbiont proliferation. High-resolution metabolic analysis confirmed that all hosts co-incorporated glucose-derived 13C and ammonium-derived 15N via glutamine synthetase–glutamate synthase-mediated amino acid biosynthesis. Our results reveal a general carbon-nitrogen negative feedback loop underlying these symbioses and provide a parsimonious explanation for their repeated evolution.

Coral larvae employ nitrogen sequestration mechanisms to stabilize carbon provisioning from algal symbionts under increased temperature

“…The authors proposed that increased coral host central carbon metabolism generates metabolites required for ammonium assimilation, leading to increased ammonium assimilation by the host and less available to the symbiont. Reduced ammonium availability for the symbiont limits growth and symbiont photosynthesis [21]. [22] provided evidence that translocation of photosynthates stimulates ammonium assimilation in the host, reducing nitrogen availability and consequently, symbiont population growth rate declines this would allow for greater translocation of excess carbon relative to the population growth rate [10,28,29,119].…”

“…The mechanisms underlying the onset and progression of coral bleaching are complex and a topic of intense scientific study (see a recent review in [19]). Research in the last two decades has demonstrated that oxidative stress [19,20], as well as carbon and nitrogen imbalance can drive dysbiosis and lead to bleaching [19,[21][22][23][24][25].…”

“…Carbon-nitrogen exchange is a core process regulating symbiotic stability [21,22,26]. Host control of nitrogen is critical to maintaining carbon translocation [9,22,26,27].…”

“…When released from nitrogen limitation, symbiont population growth increases requiring greater photosynthate retention within the symbiont, thus less is translocated to the host [7,9,27,29]. Under high temperatures, increased metabolic demand in the host and increased metabolism of lipids reserves and amino acids produces elevated nitrogenous waste, increasing nitrogen availability [9,21,28,30]. As symbiont populations grow and retain more fixed carbon and subsequently translocate less to the host [28,29], there is depletion of host energy resources [31,32], and therefore less energy available to actively sequester nitrogen [21], exacerbating nitrogen imbalance and destabilizing symbiosis [22,28].…”

“…Under high temperatures, increased metabolic demand in the host and increased metabolism of lipids reserves and amino acids produces elevated nitrogenous waste, increasing nitrogen availability [9,21,28,30]. As symbiont populations grow and retain more fixed carbon and subsequently translocate less to the host [28,29], there is depletion of host energy resources [31,32], and therefore less energy available to actively sequester nitrogen [21], exacerbating nitrogen imbalance and destabilizing symbiosis [22,28]. Under climate change conditions, the role of carbon-nitrogen exchange in maintaining stable symbioses requires further examination.…”