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1. Spatial and Temporal Patterns of Symbiont Colonization and Loss During Bleaching in the Model Sea Anemone Aiptasia

   https://doi.org/10.3389/fmars.2022.808696  

   Tivey, Trevor R.; Coleman, Tyler J.; Weis, Virginia M. (March 2022, Frontiers in Marine Science)

   The ability of symbionts to recolonize their hosts after a period of dysbiosis is essential to maintain a resilient partnership. Many cnidarians rely on photosynthate provided from a large algal symbiont population. Under periods of thermal stress, symbiont densities in host cnidarians decline, and the recovery of hosts is dependent on the re-establishment of symbiosis. The cellular mechanisms that govern this process of colonization are not well-defined and require further exploration. To study this process in the symbiotic sea anemone model Exaiptasia diaphana , commonly called Aiptasia, we developed a non-invasive, efficient method of imaging that uses autofluorescence to measure the abundance of symbiont cells, which were spatially distributed into distinct cell clusters within the gastrodermis of host tentacles. We estimated cell cluster sizes to measure the occurrence of singlets, doublets, and so on up to much larger cell clusters, and characterized colonization patterns by native and non-native symbionts. Native symbiont Breviolum minutum rapidly recolonized hosts and rapidly exited under elevated temperature, with increased bleaching susceptibility for larger symbiont clusters. In contrast, populations of non-native symbionts Symbiodinium microadriaticum and Durusdinium trenchii persisted at low levels under elevated temperature. To identify mechanisms driving colonization patterns, we simulated symbiont population changes through time and determined that migration was necessary to create observed patterns (i.e., egression of symbionts from larger clusters to establish new clusters). Our results support a mechanism where symbionts repopulate hosts in a predictable cluster pattern, and provide novel evidence that colonization requires both localized proliferation and continuous migration. 

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2. Stability of the cnidarian–dinoflagellate symbiosis is primarily determined by symbiont cell-cycle arrest

   https://doi.org/10.1073/pnas.2412396122  

   Gorman, Lucy M; Tivey, Trevor R; Raymond, Evan H; Ashley, Immy A; Oakley, Clinton A; Grossman, Arthur R; Weis, Virginia M; Davy, Simon K (April 2025, Proceedings of the National Academy of Sciences)

   Queller, David (Ed.)

   The cnidarian–dinoflagellate symbiosis relies on the regulation of resident symbiont populations to maintain biomass stability; however, the relative importance of host regulatory mechanisms [cell-cycle arrest (CC), apoptosis (AP), autophagy (AU), and expulsion (EX)] during symbiosis onset and maintenance is largely unknown. Here, we inoculated a symbiont-free (aposymbiotic) model cnidarian (Exaiptasia diaphana: “Aiptasia”) with either its native symbiont Breviolum minutum or one of three non-native symbionts: Symbiodinium microadriaticum, Cladocopium goreaui, and Durusdinium trenchii. We then measured and compared host AP, host AU, symbiont EX, and symbiont cell-cycle phase for up to a year with these different symbionts and used these discrete measurements to inform comparative models of symbiont population regulation. Our models showed a general pattern, where regulation through AP and AU is reduced after onset, followed by an overshoot of the symbiont population that requires a strong regulatory response, dealt with by strong CC and increased EX. As colonization progresses into symbiosis maintenance, CC remains crucial for achieving steady-state symbiont populations, with our models estimating that CC regulates 10-fold more cells (60 to 90%) relative to the other mechanisms. Notably though, our models also revealed that D. trenchii is less tightly regulated than B. minutum, consistent with D. trenchii’s reputation as a suboptimal partner for this cnidarian. Overall, our models suggest that single regulatory mechanisms do not accurately replicate observed symbiont colonization patterns, reflecting the importance of all mechanisms working concomitantly. This ultimately sheds light on the cell biology underpinning the stability of this ecologically significant symbiosis. 

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3. Symbiont genotype influences holobiont response to increased temperature

   https://doi.org/10.1038/s41598-022-23244-3  

   Moffat, Jennica J.; Coffroth, Mary Alice; Wallingford, Piper D.; terHorst, Casey P. (November 2022, Scientific Reports)

   Abstract As coral reefs face warming oceans and increased coral bleaching, a whitening of the coral due to loss of microalgal endosymbionts, the possibility of evolutionary rescue offers some hope for reef persistence. In tightly linked mutualisms, evolutionary rescue may occur through evolution of the host and/or endosymbionts. Many obligate mutualisms are composed of relatively small, fast-growing symbionts with greater potential to evolve on ecologically relevant time scales than their relatively large, slower growing hosts. Numerous jellyfish species harbor closely related endosymbiont taxa to other cnidarian species such as coral, and are commonly used as a model system for investigating cnidarian mutualisms. We examined the potential for adaptation of the upside-down jellyfishCassiopea xamachanato increased temperature via evolution of its microalgal endosymbiont,Symbiodinium microadriaticum. We quantified trait variation among five algal genotypes in response to three temperatures (26 °C, 30 °C, and 32 °C) and fitness of hosts infected with each genotype. All genotypes showed positive growth rates at each temperature, but rates of respiration and photosynthesis decreased with increased temperature. Responses varied among genotypes but were unrelated to genetic similarity. The effect of temperature on asexual reproduction and the timing of development in the host also depended on the genotype of the symbiont. Natural selection could favor different algal genotypes at different temperatures, affecting host fitness. This eco-evolutionary interaction may be a critical component of understanding species resilience in increasingly stressful environments. 

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4. The Effects of Temperature, Light, and Feeding on the Physiology of Pocillopora damicornis, Stylophora pistillata, and Turbinaria reniformis Corals

   https://doi.org/10.3390/w13152048  

   Dobson, Kerri L.; Ferrier-Pagès, Christine; Saup, Casey M.; Grottoli, Andréa G. (August 2021, Water)

   Evidence has shown that individually feeding or reduced light can mitigate the negative effects of elevated temperature on coral physiology. We aimed to evaluate if simultaneous low light and feeding would mitigate, minimize, or exacerbate negative effects of elevated temperature on coral physiology and carbon budgets. Pocillopora damicornis, Stylophora pistillata, and Turbinaria reniformis were grown for 28 days under a fully factorial experiment including two seawater temperatures (ambient temperature of 25 °C, elevated temperature of 30 °C), two light levels (high light of 300 μmol photons m−2 s−1, low light of 150 μmol photons m−2 s−1), and either fed (Artemia nauplii) or unfed. Coral physiology was significantly affected by temperature in all species, but the way in which low light and feeding altered their physiological responses was species-specific. All three species photo-acclimated to low light by increasing chlorophyll a. Pocillopora damicornis required feeding to meet metabolic demand irrespective of temperature but was unable to maintain calcification under low light when fed. In T. reniformis, low light mitigated the negative effect of elevated temperature on total lipids, while feeding mitigated the negative effects of elevated temperature on metabolic demand. In S. pistillata, low light compounded the negative effects of elevated temperature on metabolic demand, while feeding minimized this negative effect but was not sufficient to provide 100% metabolic demand. Overall, low light and feeding did not act synergistically, nor additively, to mitigate the negative effects of elevated temperature on P. damicornis, S. pistillata, or T. reniformis. However, feeding alone was critical to the maintenance of metabolic demand at elevated temperature, suggesting that sufficient supply of heterotrophic food sources is likely essential for corals during thermal stress (bleaching) events. 

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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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