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1. Heat challenge elicits stronger physiological and gene expression responses than starvation in symbiotic Oculina arbuscula

   https://doi.org/10.1093/jhered/esac068  

   Rivera, Hanny E ; Tramonte, Carlos A ; Samaroo, Jason ; Dickerson, Hayden ; Davies, Sarah W ( March 2023 , Journal of Heredity)

   Zamudio, Kelly (Ed.)

   Heterotrophy has been shown to mitigate coral–algal dysbiosis (coral bleaching) under heat challenge, but the molecular mechanisms underlying this phenomenon remain largely unexplored. Here, we quantified coral physiology and gene expression of fragments from 13 genotypes of symbiotic Oculina arbuscula after a 28-d feeding experiment under (1) fed, ambient (24 °C); (2) unfed, ambient; (3) fed, heated (ramp to 33 °C); and (4) unfed, heated treatments. We monitored algal photosynthetic efficiency throughout the experiment, and after 28 d, profiled coral and algal carbohydrate and protein reserves, coral gene expression, algal cell densities, and chlorophyll-a and chlorophyll-c2 pigments. Contrary to previous findings, heterotrophy did little to mitigate the impacts of temperature, and we observed few significant differences in physiology between fed and unfed corals under heat challenge. Our results suggest the duration and intensity of starvation and thermal challenge play meaningful roles in coral energetics and stress response; future work exploring these thresholds and how they may impact coral responses under changing climate is urgently needed. Gene expression patterns under heat challenge in fed and unfed corals showed gene ontology enrichment patterns consistent with classic signatures of the environmental stress response. While gene expression differences between fed and unfed corals under heat challenge were subtle: Unfed, heated corals uniquely upregulated genes associated with cell cycle functions, an indication that starvation may induce the previously described, milder “type B” coral stress response. Future studies interested in disentangling the influence of heterotrophy on coral bleaching would benefit from leveraging the facultative species studied here, but using the coral in its symbiotic and aposymbiotic states.

    

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2. Symbiosis modulates gene expression of symbionts, but not coral hosts, under thermal challenge

   https://doi.org/10.1111/mec.17318  

   Aichelman, Hannah E. ; Huzar, Alexa K. ; Wuitchik, Daniel M. ; Atherton, Kathryn F. ; Wright, Rachel M. ; Dixon, Groves ; Schlatter, E. ; Haftel, Nicole ; Davies, Sarah W. ( March 2024 , Molecular Ecology)

   Increasing ocean temperatures are causing dysbiosis between coral hosts and their symbionts. Previous work suggests that coral host gene expression responds more strongly to environmental stress compared to their intracellular symbionts; however, the causes and consequences of this phenomenon remain untested. We hypothesized that symbionts are less responsive because hosts modulate symbiont environments to buffer stress. To test this hypothesis, we leveraged the facultative symbiosis between the scleractinian coralOculina arbusculaand its symbiontBreviolum psygmophilumto characterize gene expression responses of both symbiotic partners in and ex hospite under thermal challenges. To characterize host and in hospite symbiont responses, symbiotic and aposymbioticO. arbusculawere exposed to three treatments: (1) control (18°C), (2) heat (32°C), and (3) cold (6°C). This experiment was replicated withB. psygmophilumcultured fromO. arbusculato characterize ex hospite symbiont responses. Both thermal challenges elicited classic environmental stress responses (ESRs) inO. arbuscularegardless of symbiotic state, with hosts responding more strongly to cold challenge. Hosts also exhibited stronger responses than in hospite symbionts. In and ex hospiteB. psygmophilumboth down‐regulated gene ontology pathways associated with photosynthesis under thermal challenge; however, ex hospite symbionts exhibited greater gene expression plasticity and differential expression of genes associated with ESRs. Taken together, these findings suggest thatO. arbusculahosts may buffer environments ofB. psygmophilumsymbionts; however, we outline the future work needed to confirm this hypothesis.

    

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3. Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity

   https://doi.org/10.1038/s41598-021-00697-6  

   Rivera, H. E. ; Davies, S. W. ( December 2021 , Scientific Reports)

   Abstract Symbiosis with unicellular algae in the family Symbiodiniaceae is common across tropical marine invertebrates. Reef-building corals offer a clear example of cellular dysfunction leading to a dysbiosis that disrupts entire ecosystems in a process termed coral bleaching. Due to their obligate symbiotic relationship, understanding the molecular underpinnings that sustain this symbiosis in tropical reef-building corals is challenging, as any aposymbiotic state is inherently coupled with severe physiological stress. Here, we leverage the subtropical, facultatively symbiotic and calcifying coral Oculina arbuscula to investigate gene expression differences between aposymbiotic and symbiotic branches within the same colonies under baseline conditions. We further compare gene ontology (GO) and KOG enrichment in gene expression patterns from O. arbuscula with prior work in the sea anemone Exaiptasia pallida (Aiptasia) and the salamander Ambystoma maculatum —both of which exhibit endophotosymbiosis with unicellular algae. We identify nitrogen cycling, cell cycle control, and immune responses as key pathways involved in the maintenance of symbiosis under baseline conditions. Understanding the mechanisms that sustain a healthy symbiosis between corals and Symbiodiniaceae algae is of urgent importance given the vulnerability of these partnerships to changing environmental conditions and their role in the continued functioning of critical and highly diverse marine ecosystems. 

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4. Importance of depth and temperature variability as drivers of coral symbiont composition despite a mass bleaching event

   https://doi.org/10.1038/s41598-023-35425-9  

   de Souza, Mariana Rocha ; Caruso, Carlo ; Ruiz-Jones, Lupita ; Drury, Crawford ; Gates, Ruth D. ; Toonen, Robert J. ( December 2023 , Scientific Reports)

   Abstract Coral reefs are iconic examples of climate change impacts because climate-induced heat stress causes the breakdown of the coral-algal symbiosis leading to a spectacular loss of color, termed ‘coral bleaching’. To examine the fine-scale dynamics of this process, we re-sampled 600 individually marked Montipora capitata colonies from across Kāne’ohe Bay, Hawai’i and compared the algal symbiont composition before and after the 2019 bleaching event. The relative proportion of the heat-tolerant symbiont Durusdinium in corals increased in most parts of the bay following the bleaching event. Despite this widespread increase in abundance of Durusdinium , the overall algal symbiont community composition was largely unchanged, and hydrodynamically defined regions of the bay retained their distinct pre-bleaching compositions. We explain ~ 21% of the total variation, of which depth and temperature variability were the most significant environmental drivers of Symbiodiniaceae community composition by site regardless of bleaching intensity or change in relative proportion of Durusdinium . We hypothesize that the plasticity of symbiont composition in corals may be constrained to adaptively match the long-term environmental conditions surrounding the holobiont, despite an individual coral’s stress and bleaching response. 

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5. Going with the flow: How corals in high‐flow environments can beat the heat

   https://doi.org/10.1111/mec.15869  

   Fifer, James ; Bentlage, Bastian ; Lemer, Sarah ; Fujimura, Atsushi G. ; Sweet, Michael ; Raymundo, Laurie J. ( March 2021 , Molecular Ecology)

   Coral reefs are experiencing unprecedented declines in health on a global scale leading to severe reductions in coral cover. One major cause of this decline is increasing sea surface temperature. However, conspecific colonies separated by even small spatial distances appear to show varying responses to this global stressor. One factor contributing to differential responses to heat stress is variability in the coral's micro‐environment, such as the amount of water flow a coral experiences. High flow provides corals with a variety of health benefits, including heat stress mitigation. Here, we investigate how water flow affects coral gene expression and provides resilience to increasing temperatures. We examined host and photosymbiont gene expression ofAcroporacf.pulchracolonies in discrete in situ flow environments during a natural bleaching event. In addition, we conducted controlled ex situ tank experiments where we exposedA. cf.pulchrato different flow regimes and acute heat stress. Notably, we observed distinct flow‐driven transcriptomic signatures related to energy expenditure, growth, heterotrophy and a healthy coral host–photosymbiont relationship. We also observed disparate transcriptomic responses during bleaching recovery between the high‐ and low‐flow sites. Additionally, corals exposed to high flow showed “frontloading” of specific heat‐stress‐related genes such as heat shock proteins, antioxidant enzymes, genes involved in apoptosis regulation, innate immunity and cell adhesion. We posit that frontloading is a result of increased oxidative metabolism generated by the increased water movement. Gene frontloading may at least partially explain the observation that colonies in high‐flow environments show higher survival and/or faster recovery in response to bleaching events.

    

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