Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions

Hypoxia Routes Tryptophan Homeostasis Towards Increased Tryptamine Production

The liver is the central hub for processing and maintaining homeostatic levels of dietary nutrients especially essential amino acids such as tryptophan (Trp). Trp is required not only to sustain protein synthesis but also as a precursor for the production of NAD, neurotransmitters and immunosuppressive metabolites. In light of these roles of Trp and its metabolic products, maintaining homeostatic levels of Trp is essential for health and well-being. The liver regulates global Trp supply by the immunosuppressive enzyme tryptophan-2,3-dioxygenase (TDO2), which degrades Trp down the kynurenine pathway (KP). In the current study, we show that isolated primary hepatocytes when exposed to hypoxic environments, extensively rewire their Trp metabolism by reducing constitutive Tdo2 expression and differentially regulating other Trp pathway enzymes and transporters. Mathematical modelling of Trp metabolism in liver cells under hypoxia predicted decreased flux through the KP while metabolic flux through the tryptamine branch significantly increased. In line, the model also revealed an increased accumulation of tryptamines under hypoxia, at the expense of kynurenines. Metabolic measurements in hypoxic hepatocytes confirmed the predicted reduction in KP metabolites as well as accumulation of tryptamine. Tdo2 expression in cultured primary hepatocytes was reduced upon hypoxia inducible factor (HIF) stabilisation by dimethyloxalylglycine (DMOG), demonstrating that HIFs are involved in the hypoxic downregulation of hepatic Tdo2. DMOG abrogated hepatic luciferase signals in Tdo2 reporter mice, indicating that HIF stability also recapitulates hypoxic rewiring of Trp metabolism in vivo. Also in WT mice HIF stabilization drove homeostatic Trp metabolism away from the KP towards enhanced tryptamine production, leading to enhanced levels of tryptamine in liver, serum and brain. As tryptamines are the most potent hallucinogens known, the observed upregulation of tryptamine in response to hypoxic exposure of hepatocytes may be involved in the generation of hallucinations occurring at high altitude. KP metabolites are known to activate the aryl hydrocarbon receptor (AHR). The AHR-activating properties of tryptamines may explain why immunosuppressive AHR activity is maintained under hypoxia despite downregulation of the KP. In summary our results identify hypoxia as an important factor controlling Trp metabolism in the liver with possible implications for immunosuppressive AHR activation and mental disturbances

Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

Efficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.Peer reviewe

A Salty Coral Secret : How High Salinity Helps Corals To Be Stronger

Corals are mysterious animals that have been around for ages. They are the creators of beautiful reefs. Sadly, the reefs that we love to look at are in danger of overheating and are disappearing from our planet. While this sounds bad, not all corals are affected the same way by warm seawater. Corals from the Red Sea seem to be more resistant to higher temperatures than are corals from other regions. Red Sea reefs are thriving in seawater that is hotter than that in other places. But what is their secret? What makes Red Sea corals stronger and more heat resistant? We know that Red Sea corals not only handle the incredibly high temperatures, but also deal with high salinity (saltiness). This connection between high salinity and high temperature made us wonder: can we find evidence that high salinity makes corals stronger?publishe

Carbohydrate composition of mucus from scleractinian corals from the central Red Sea

Coral mucus is continuously released by most corals and acts as an important protective barrier and as a substrate for host-associated microbial communities due to its complex composition of carbohydrates, lipids, and proteins. On a reef scale, coral mucus functions as a particle trap, thereby retaining nutrients and energy in the ecosystem. Given the distinct environmental conditions in the Red Sea (high temperature, high salinity, high total alkalinity), we sought to investigate the carbohydrate composition of mucus from five corals from the central Red Sea. Our aim was to assess whether mucus from Red Sea corals is different from what is known from other corals and whether those differences could be aligned to putative beneficial functions with regard to the prevailing environment. Using gas chromatography/mass spectrometry, we detected nine sugars as the main prevalent carbohydrates. Although we detected significant differences between species with regard to the relative abundance of given carbohydrates, the identified sugars resembled those found in mucus from corals elsewhere, and we could corroborate high abundance of arabinose in acroporid corals. Taken together, our results suggest the presence of a common set of carbohydrates across a broad range of coral species from geographically diverse environments, highlighting the important role of mucus with regard to coral and reef ecosystem function.publishe

Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome

Coral bleaching, i.e., the loss of photosynthetic algal endosymbionts, caused by ocean warming is now among the main factors driving global reef decline, making the elucidation of factors that contribute to thermotolerance important. Recent studies implicate high salinity as a contributing factor in cnidarians, potentially explaining the high thermotolerance of corals from the Arabian Seas. Here we characterized bacterial community composition under heat stress at different salinities using the coral model Aiptasia. Exposure of two Aiptasia host-algal symbiont pairings (H2-SSB01 and CC7-SSA01) to ambient (25°C) and heat stress (34°C) temperatures at low (36 PSU), intermediate (39 PSU), and high (42 PSU) salinities showed that bacterial community composition at high salinity was significantly different, concomitant with reduced bleaching susceptibility in H2-SSB01, not observed in CC7-SSA01. Elucidation of bacteria that showed increased relative abundance at high salinity, irrespective of heat stress, revealed candidate taxa that could potentially contribute to the observed increased thermotolerance. We identified 4 (H2-SSB01) and 3 (CC7-SSA01) bacterial taxa belonging to the orders Alteromonadales (1 OTU), Oligoflexales (1 OTU), Rhizobiales (2 OTUs), and Rhodobacterales (2 OTUs), suggesting that only few bacterial taxa are potential contributors to an increase in thermal tolerance at high salinities. These taxa have previously been implicated in nitrogen and DMSP cycling, processes that are considered to affect thermotolerance. Our study demonstrates microbiome restructuring in symbiotic cnidarians under heat stress at different salinities. As such, it underlines how host-associated bacterial communities adapt to prevailing environmental conditions with putative consequences for the environmental stress tolerance of the emergent metaorganism.publishe

The genome of the cauliflower coral Pocillopora verrucosa

Climate change and ocean warming threaten the persistence of corals worldwide. Genomic resources are critical to study the evolutionary trajectory, adaptive potential, and genetic distinctiveness of coral species. Here we provide a reference genome of the cauliflower coral Pocillopora verrucosa, a broadly prevalent reef-building coral with important ecological roles in the maintenance of reefs across the Red Sea, the Indian Ocean, and the Pacific Ocean. The genome has an assembly size of 380,505,698 bp with a scaffold N50 of 333,696 bp and a contig N50 of 75,704 bp. The annotation of the assembled genome returned 27,439 gene models of which 89.88% have evidence of transcription from RNA-Seq data and 97.87% show homology to known genes. A high proportion of the genome (41.22%) is comprised of repetitive elements in comparison to other cnidarian genomes, in particular in relation to the small genome size of P. verrucosa.publishe

High salinity conveys thermotolerance in the coral model Aiptasia

The endosymbiosis between dinoflagellate algae of the genus Symbiodinium and stony corals provides the foundation of coral reef ecosystems. Coral bleaching, the expulsion of endosymbionts from the coral host tissue as a consequence of heat or light stress, poses a threat to reef ecosystem functioning on a global scale. Hence, a better understanding of the factors contributing to heat stress susceptibility and tolerance is needed. In this regard, some of the most thermotolerant corals live in particularly saline habitats, but possible effects of high salinity on thermotolerance in corals are anecdotal. Here we test the hypothesis that high salinity may lead to increased thermotolerance. We conducted a heat stress experiment at low, intermediate, and high salinities using a set of host-endosymbiont combinations of the coral model Aiptasia. As expected, all host-endosymbiont combinations showed reduced photosynthetic efficiency and endosymbiont loss during heat stress, but the severity of bleaching was significantly reduced with increasing salinities for one of the host-endosymbiont combinations. Our results show that higher salinities can convey increased thermotolerance in Aiptasia, although this effect seems to be dependent on the particular host strain and/or associated symbiont type. This finding may help explain the extraordinarily high thermotolerance of corals in high salinity environments, such as the Red Sea and the Persian/Arabian Gulf, and provides novel insight regarding factors that contribute to thermotolerance. Since our results are based on a salinity effect in symbiotic sea anemones, it remains to be determined whether this salinity effect can also be observed in stony corals.publishe

Heat stress destabilizes symbiotic nutrient cycling in corals

Recurrent mass bleaching events are pushing coral reefs world-wide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral-algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the break-down of the coral-algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral-algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.Peer reviewe

High levels of floridoside at high salinity link osmoadaptation with bleaching susceptibility in the cnidarian-algal endosymbiosis

Coral reefs are in global decline mainly due to increasing sea surface temperatures triggering coral bleaching. Recently, high salinity has been linked to increased thermotolerance and decreased bleaching in the sea anemone coral model Aiptasia. However, the underlying processes remain elusive. Using two Aiptasia host­–endosymbiont pairings, we induced bleaching at different salinities and show reduced reactive oxygen species (ROS) release at high salinities, suggesting a role of osmoadaptation in increased thermotolerance. A subsequent screening of osmolytes revealed that this effect was only observed in algal endosymbionts that produce 2-O-glycerol-α-D-galactopyranoside (floridoside), an osmolyte capable of scavenging ROS. This result argues for a mechanistic link between osmoadaptation and thermotolerance, mediated by ROS-scavenging osmolytes (e.g., floridoside). This sheds new light on the putative mechanisms underlying the remarkable thermotolerance of corals from water bodies with high salinity such as the Red Sea or Persian/Arabian Gulf and holds implications for coral thermotolerance under climate change.publishe