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1. Coral larvae increase nitrogen assimilation to stabilize algal symbiosis and combat bleaching under increased temperature

   https://doi.org/10.1371/journal.pbio.3002875  

   Huffmyer, Ariana S; Ashey, Jill; Strand, Emma; Chiles, Eric N; Su, Xiaoyang; Putnam, Hollie M (November 2024, PLOS Biology)

   Moran, Nancy A (Ed.)

   Rising sea surface temperatures are increasingly causing breakdown in the nutritional relationship between corals and algal endosymbionts (Symbiodiniaceae), threatening the basis of coral reef ecosystems and highlighting the critical role of coral reproduction in reef maintenance. The effects of thermal stress on metabolic exchange (i.e., transfer of fixed carbon photosynthates from symbiont to host) during sensitive early life stages, however, remains understudied. We exposed symbiotic Montipora capitata coral larvae in Hawaiʻi to high temperature (+2.5°C for 3 days), assessed rates of photosynthesis and respiration, and used stable isotope tracing (4 mM 13C sodium bicarbonate; 4.5 h) to quantify metabolite exchange. While larvae did not show any signs of bleaching and did not experience declines in survival and settlement, metabolic depression was significant under high temperature, indicated by a 19% reduction in respiration rates, but with no change in photosynthesis. Larvae exposed to high temperature showed evidence for maintained translocation of a major photosynthate, glucose, from the symbiont, but there was reduced metabolism of glucose through central carbon metabolism (i.e., glycolysis). The larval host invested in nitrogen cycling by increasing ammonium assimilation, urea metabolism, and sequestration of nitrogen into dipeptides, a mechanism that may support the maintenance of glucose translocation under thermal stress. Host nitrogen assimilation via dipeptide synthesis appears to be used for nitrogen limitation to the Symbiodiniaceae, and we hypothesize that nitrogen limitation contributes to retention of fixed carbon by favoring photosynthate translocation to the host. Collectively, our findings indicate that although these larvae are susceptible to metabolic stress under high temperature, diverting energy to nitrogen assimilation to maintain symbiont population density, photosynthesis, and carbon translocation may allow larvae to avoid bleaching and highlights potential life stage specific metabolic responses to stress. 

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2. Metabolomic shifts associated with heat stress in coral holobionts

   https://doi.org/10.1126/sciadv.abd4210  

   Williams, Amanda; Chiles, Eric N.; Conetta, Dennis; Pathmanathan, Jananan S.; Cleves, Phillip A.; Putnam, Hollie M.; Su, Xiaoyang; Bhattacharya, Debashish (January 2021, Science Advances)

   null (Ed.)

   Understanding the response of the coral holobiont to environmental change is crucial to inform conservation efforts. The most pressing problem is “coral bleaching,” usually precipitated by prolonged thermal stress. We used untargeted, polar metabolite profiling to investigate the physiological response of the coral species Montipora capitata and Pocillopora acuta to heat stress. Our goal was to identify diagnostic markers present early in the bleaching response. From the untargeted UHPLC-MS data, a variety of co-regulated dipeptides were found that have the highest differential accumulation in both species. The structures of four dipeptides were determined and showed differential accumulation in symbiotic and aposymbiotic (alga-free) populations of the sea anemone Aiptasia ( Exaiptasia pallida ), suggesting the deep evolutionary origins of these dipeptides and their involvement in symbiosis. These and other metabolites may be used as diagnostic markers for thermal stress in wild coral. 

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3. Metabolomic shifts associated with heat stress in coral holobionts

   https://doi.org/doi:10.1126/sciadv.abd4210  

   Amanda Williams, Eric N. (January 2021, Science advances)

   null (Ed.)

   Understanding the response of the coral holobiont to environmental change is crucial to inform conservation efforts. The most pressing problem is “coral bleaching,” usually precipitated by prolonged thermal stress. We used untargeted, polar metabolite profiling to investigate the physiological response of the coral species Montipora capitata and Pocillopora acuta to heat stress. Our goal was to identify diagnostic markers present early in the bleaching response. From the untargeted UHPLC-MS data, a variety of co-regulated dipeptides were found that have the highest differential accumulation in both species. The structures of four dipeptides were determined and showed differential accumulation in symbiotic and aposymbiotic (alga-free) populations of the sea anemone Aiptasia (Exaiptasia pallida), suggesting the deep evolutionary origins of these dipeptides and their involvement in symbiosis. These and other metabolites may be used as diagnostic markers for thermal stress in wild coral. 

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4. Divergent responses of the coral holobiont to deoxygenation and prior environmental stress

   https://doi.org/10.3389/fmars.2023.1301474  

   Swaminathan, Sara D.; Meyer, Julie L.; Johnson, Maggie D.; Paul, Valerie J.; Bartels, Erich; Altieri, Andrew H. (February 2024, Frontiers in Marine Science)

   Ocean deoxygenation is intensifying globally due to human activities – and is emerging as a grave threat to coral reef ecosystems where it can cause coral bleaching and mass mortality. However, deoxygenation is one of many threats to coral reefs, making it essential to understand how prior environmental stress may influence responses to deoxygenation. To address this question, we examined responses of the coral holobiont (i.e., the coral host, Symbiodiniaceae, and the microbiome) to deoxygenation in corals with different environmental stress backgrounds. We outplantedAcropora cervicornisfragments of known genotypes from anin situnursery to two sites in the Florida Keys spanning an inshore-offshore gradient. After four months, fragments from the outplanted corals were transferred to the laboratory, where we tested differences in survivorship, tissue loss, photosynthetic efficiency, Symbiodiniaceae cell density, and coral microbiome composition after persistent exposure to one of four oxygen treatments ranging from extreme deoxygenation (0.5 mg L^-1) to normoxia (6 mg L^-1). We found that, for the short duration of exposure tested in this study (four days), the entire coral holobiont was resistant to dissolved oxygen (DO) concentrations as low as 2.0 mg L^-1, but that the responses of members of the holobiont decoupled at 0.5 mg L^-1. In this most extreme treatment, the coral host showed decreased photosynthetic efficiency, tissue loss, and mortality, and lower Symbiodiniaceae densities in a bleaching response, but most microbial taxa remained stable. Although deoxygenation did not cause major community shifts in microbiome composition, the population abundance of some microbial taxa did respond. Site history influenced some responses of the coral host and endosymbiont, but not the coral microbiome, with corals from the more stressful inshore site showing greater susceptibility to subsequent deoxygenation. Our study reveals that coral holobiont members respond differently to deoxygenation, with greater sensitivity in the coral host and Symbiodiniaceae and greater resistance in the coral microbiome, and that prior stress exposure can decrease host tolerance to deoxygenation. 

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5. Coral trophic pathways impact the allocation of carbon and nitrogen for egg development after bleaching

   https://doi.org/10.3389/fevo.2023.1251220  

   Jaffe, Melissa D; Padilla-Gamiño, Jacqueline L; Nunn, Brook L; Rodrigues, Lisa J (November 2023, Frontiers in Ecology and Evolution)

   The persistence of coral reefs requires the survival of adult coral colonies and their continued sexual reproduction despite thermal stress. To assess the trophic pathway (i.e., autotrophy and/or heterotrophy) used to develop gametes following bleaching, we thermally stressedMontipora capitatafor one month at a time when corals in Hawai’i typically experience elevated seawater temperatures. After six and nine months of recovery, we pulse-chased non-bleached and previously bleached colonies using a dual-label design to compare the allocation of carbon and nitrogen at significant stages of gamete development. Dissolved inorganic carbon- (DI¹³C) and nitrogen- (DI¹⁵N) labelled seawater or¹³C- and¹⁵N-labelled rotifers were used to assess the autotrophic and heterotrophic pathways, respectively. At multiple time points for up to two years later, we collected adult coral fragments and isolated host tissue, Symbiodiniaceae cells, and developing eggs and captured gamete bundles to analyze their carbon (δ¹³C) and nitrogen (δ¹⁵N) stable isotopes. We found that the presence of Symbiodiniaceae was important for gametogenesis in both non-bleached and previously bleached colonies in two main ways. First, autotrophically-acquired carbon and nitrogen were both allocated to gametes during development, suggesting that recovery of photosynthesis after bleaching is critical for gametogenesis. Second, only heterotrophically-acquired nitrogen, not carbon, was incorporated into gametes and was readily recycled between host tissues and Symbiodiniaceae cells. This suggests that one of the purposes of heterotrophy following coral bleaching forM. capitatamay be to supplement the nitrogen pool, providing available nutrients for endosymbiotic algal growth. Allocation of carbon and nitrogen to eggs coincided with the period when vertical transmission of symbionts to gametes occurs, further supporting the important relationship between gametogenesis and availability of Symbiodiniaceae forM. capitata. 

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