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1. 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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2. Sublethal changes to coral metabolism in response to deoxygenation

   https://doi.org/10.1242/jeb.249638  

   Mallon, J E; Altieri, A H; Cyronak, T; Melendez-Declet, C V; Paul, V J; Johnson, M D (February 2025, Journal of Experimental Biology)

   ABSTRACT Coastal deoxygenation poses a critical threat to tropical coral reefs. Dissolved oxygen (DO) depletion can cause hypoxia-induced stress and mortality in scleractinian corals. Coral hypoxic responses are species-specific and likely modulated by the duration and severity of low-DO conditions, although the physiological mechanisms driving hypoxia tolerance are not fully understood. In this study, the Caribbean corals Acropora cervicornis, Porites astreoides and Siderastrea siderea were exposed to either severe (1.5 mg l−1 DO) or moderate (3.5 mg l−1 DO) deoxygenation or a control treatment (6 mg l−1 DO). All corals survived 2 weeks of deoxygenation but exhibited sublethal changes to coral metabolism after 1- and 2-week exposures, compared with controls. Maximum quantum yield (Fv/Fm) was suppressed after 1 week in both deoxygenation treatments in A. cervicornis, and after 2 weeks in S. siderea and P. astreoides exposed to severe or moderate treatments, respectively. Respiration rates were lower than controls in A. cervicornis and S. siderea after 1 and 2 weeks of severe deoxygenation. The reduced respiration of P. astreoides after 1 week of moderate deoxygenation returned to control levels in week 2. Overall coral metabolic budgets, assessed by ratios of gross photosynthesis to respiration (Pg:R), were more autotrophic, or photosynthesis-dominant, after 1 week of severe deoxygenation in S. siderea and P. astreoides, whereas Pg:R was not significantly different in A. cervicornis between treatments. These results reveal that some corals shift their metabolism to tolerate low-oxygen conditions and avoid bleaching or mortality, indicating that metabolic plasticity is an important aspect of coral resistance to deoxygenation. 

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3. Locally Adapted Coral Species Withstand a 2-Week Hypoxic Event

   https://doi.org/10.3390/oceans6010005  

   Lucey, Noelle; César-Ávila, Carolina; Eckert, Alaina; Veintimilla, Paul; Collin, Rachel (March 2025, Oceans)

   NA (Ed.)

   One approach to improve long-term coral restoration success utilizes naturally stress-tolerant corals from the wild. While the focus has primarily been on thermal stress, low oxygen is a growing threat to coral reefs and restoration efforts should also consider hypoxia tolerance. Here we determine if Siderastrea siderea and Agaricia tenuifolia populations from a reef with a historical record of low oxygen exhibit evidence of local adaptation to hypoxic events, compared to populations from a reference reef. We employed a laboratory-based reciprocal transplant experiment mimicking a severe 14-night hypoxic event and monitored bleaching responses, photo-physiology, metabolic rates, and survival of all four populations during, and for two weeks following the event. In both species, we found the populations from the hypoxic reef either fully persisted or recovered within 3 days of the event. In contrast, the conspecific naïve populations from the well-oxygenated reference reef experienced bleaching and death. This showcases the vulnerability of naïve corals exposed to low oxygen but also suggests that corals from the hypoxic reef locally adapted to survive severe episodic hypoxia. Other reefs with past episodic low oxygen may also be home to corals with adaptation signatures to hypoxia and may be useful for restoration efforts. 

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4. Legacy Effects of an Extreme Marine Heatwave on a Stress‐Tolerant Coral

   https://doi.org/10.1111/gcb.70853  

   Glass, Benjamin H; Aichelman, Hannah E; Grupstra, Carsten_G B; Valadez‐Ingersoll, Maria; Swank, Ally; Guerra, Viviana; Gondola, Plinio; Nagree, Aden; Schipfer, James; Gilmore, Thomas D; et al (April 2026, Global Change Biology)

   ABSTRACT During the 4th Global Coral Bleaching Event (GCBE4; January 2023–September 2025), an extreme marine heatwave occurred on the Bocas del Toro Reef Complex (BTRC) in Panama. We characterized how this heatwave impacted the health and holobiont communities of the stress‐tolerant coralSiderastrea sidereaat four sites across the BTRC. Tagged colonies at each site (N = 30–53 colonies per site) were visited before, during, and after the heatwave (early May 2022, mid‐August 2023, and late April 2024, respectively), and images and DNA samples were collected at each time point. In situ temperature logger data showed that sites reached maxima of 32.1°C–33.9°C in October 2023, resulting in the accumulation of ~12–20 maximum degree‐heating weeks (DHWs). Consequently,S. sidereacolonies displayed widespread bleaching (i.e., the loss of algal endosymbionts), with an increase from 8.6% to 33% of colonies bleached per site in May 2022 to 33%–70% in August 2023, followed by a decline to 15%–63% by April 2024. Colony‐level partial mortality increased significantly between 2022 and 2024 at three of the four sites, and was observed even in colonies that were not bleached in August 2023. Further, many corals hostingCladocopiumspp. algal symbionts in 2022 shifted towards less diverse communities dominated by heat‐tolerantBreviolumandDurusdiniumspp., and most of these corals continued to host modified symbiont communities for months. The heatwave also reshaped corals' bacterial microbiomes, including increases in α‐diversity and abundances of potentially pathogenic taxa (e.g., Vibrionaceae), and these shifts were persistent following the heatwave. Together, these findings demonstrate that GCBE4 had lasting impacts onS. sidereaholobiont health across the BTRC, underscoring that extreme heat events can compromise even stress‐tolerant coral species and induce legacy effects that will likely affect their future resilience. Rapid action to minimize further ocean warming is thus necessary to safeguard reef ecosystems. 

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5. Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality

   https://doi.org/10.1111/gcb.17088  

   Vompe, Alex D; Epstein, Hannah E; Speare, Kelly E; Schmeltzer, Emily R; Adam, Thomas C; Burkepile, Deron E; Sharpton, Thomas J; Vega Thurber, Rebecca (January 2024, Global Change Biology)

   Abstract Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large‐scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long‐term (28 months, 2018–2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves inAcropora retusa,Porites lobata, andPocilloporaspp., which included: microbiome acclimatization inA. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave inPocilloporaspp. Moreover, observed microbiome dynamics significantly correlated with coral species‐specific phenotypes. For example, bleaching and mortality inA. retusaboth significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, whileP. lobatacolonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality inA. retusa. This study reveals evidence for coral species‐specific microbial responses to repeated heatwaves and, importantly, suggests that host‐dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress. 

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