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1. 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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2. Groundtruthing nitrogen isotopes as a symbiosis proxy using the facultatively symbiotic coral Oculina arbuscula

   https://doi.org/10.3389/fmars.2024.1433382  

   Donnelly, Heather A; Valadez-Ingersoll, Maria; Lin, Marcus; Rivera, Hanny E; Tramonte, Carlos A; Davies, Sarah W; Wang, Xingchen Tony (August 2024, Frontiers in Marine Science)

   The resilience of coral reefs in oligotrophic, (sub)tropical oceans is largely due to the symbiotic relationship between scleractinian corals and Symbiodiniaceae algae, which enables efficient internal nutrient recycling. Investigating the history of this coral symbiosis can provide insights into its role in sustaining the health of both present and future coral reefs. The isotopic composition of organic nitrogen (¹⁵N/¹⁴N or δ¹⁵N) bound within coral skeletons has been utilized to trace the existence of symbiosis in fossil corals, suggesting that coral symbiosis dates back to at least 210 million years ago. The basis of this proxy is that symbiotic corals are expected to exhibit lower δ¹⁵N compared to their non-symbiotic (aposymbiotic) counterparts within the same environments, owing to internal nitrogen recycling between the coral host and algal symbiont, and reduced leakage of low-δ¹⁵N ammonium into seawater. However, this hypothesis has not been adequately tested in contemporary settings. In a laboratory experiment, we examined the δ¹⁵N differences between the symbiotic and aposymbiotic branches within the same genetic backgrounds of the facultatively symbiotic coralOculina arbusculaunder well-fed conditions. Across five different genotypes in two separate experiments, symbiotic branches consistently showed lower δ¹⁵N than their aposymbiotic counterparts. These findings corroborate the use of δ¹⁵N as a proxy for identifying coral symbiosis in the past, particularly when multiple species of corals coexisted in the same environments. 

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3. Energy Sources of the Depth-Generalist Mixotrophic Coral Stylophora pistillata

   https://doi.org/10.3389/fmars.2020.566663  

   Martinez, Stephane; Kolodny, Yuval; Shemesh, Eli; Scucchia, Federica; Nevo, Reinat; Levin-Zaidman, Smadar; Paltiel, Yossi; Keren, Nir; Tchernov, Dan; Mass, Tali (November 2020, Frontiers in Marine Science)

   null (Ed.)

   Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30–150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ 15 N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a , lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial. 

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4. Analysis of a mechanistic model of corals in association with multiple symbionts: within-host competition and recovery from bleaching

   https://doi.org/10.1093/conphys/coac066  

   Brown, Alexandra Lynne; Pfab, Ferdinand; Baxter, Ethan C; Detmer, A Raine; Moeller, Holly V; Nisbet, Roger M; Cunning, Ross (January 2022, Conservation Physiology)

   Cooke, Steven (Ed.)

   Abstract Coral reefs are increasingly experiencing stressful conditions, such as high temperatures, that cause corals to undergo bleaching, a process where they lose their photosynthetic algal symbionts. Bleaching threatens both corals’ survival and the health of the reef ecosystems they create. One possible mechanism for corals to resist bleaching is through association with stress-tolerant symbionts, which are resistant to bleaching but may be worse partners in mild conditions. Some corals have been found to associate with multiple symbiont species simultaneously, which potentially gives them access to the benefits of both stress-sensitive and -tolerant symbionts. However, within-host competition between symbionts may lead to competitive exclusion of one partner, and the consequences of associating with multiple partners simultaneously are not well understood. We modify a mechanistic model of coral-algal symbiosis to investigate the effect of environmental conditions on within-host competitive dynamics between stress-sensitive and -tolerant symbionts and the effect of access to a tolerant symbiont on the dynamics of recovery from bleaching. We found that the addition of a tolerant symbiont can increase host survival and recovery from bleaching in high-light conditions. Competitive exclusion of the tolerant symbiont occurred slowly at intermediate light levels. Interestingly, there were some cases of post-bleaching competitive exclusion after the tolerant symbiont had helped the host recover. 

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5. Thermotolerant coral–algal mutualisms maintain high rates of nutrient transfer while exposed to heat stress

   https://doi.org/10.1098/rspb.2023.1403  

   Kemp, Dustin W.; Hoadley, Kenneth D.; Lewis, Allison M.; Wham, Drew C.; Smith, Robin T.; Warner, Mark E.; LaJeunesse, Todd C. (September 2023, Proceedings of the Royal Society B: Biological Sciences)

   Symbiotic mutualisms are essential to ecosystems and numerous species across the tree of life. For reef-building corals, the benefits of their association with endosymbiotic dinoflagellates differ within and across taxa, and nutrient exchange between these partners is influenced by environmental conditions. Furthermore, it is widely assumed that corals associated with symbionts in the genusDurusdiniumtolerate high thermal stress at the expense of lower nutrient exchange to support coral growth. We traced both inorganic carbon (H¹³CO₃^–) and nitrate (¹⁵NO₃^–) uptake by divergent symbiont species and quantified nutrient transfer to the host coral under normal temperatures as well as in colonies exposed to high thermal stress. Colonies representative of diverse coral taxa associated withDurusdinium trenchiiorCladocopiumspp. exhibited similar nutrient exchange under ambient conditions. By contrast, heat-exposed colonies withD. trenchiiexperienced less physiological stress than conspecifics withCladocopiumspp. while high carbon assimilation and nutrient transfer to the host was maintained. This discovery differs from the prevailing notion that these mutualisms inevitably suffer trade-offs in physiological performance. These findings emphasize that many host–symbiont combinations adapted to high-temperature equatorial environments are high-functioning mutualisms; and why their increased prevalence is likely to be important to the future productivity and stability of coral reef ecosystems. 

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