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 in
This content will become publicly available on February 1, 2025
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 outplanted
- Award ID(s):
- 2048914
- NSF-PAR ID:
- 10495084
- Publisher / Repository:
- Frontiers Media SA
- Date Published:
- Journal Name:
- Frontiers in Marine Science
- Volume:
- 10
- ISSN:
- 2296-7745
- Subject(s) / Keyword(s):
- ["coral reef, hypoxia, temperature, microbiome, multi-stressor, resilience, symbiosis, environmental stress"]
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Acropora retusa ,Porites lobata , andPocillopora spp., which included: microbiome acclimatization inA. retusa , and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave inPocillopora spp. Moreover, observed microbiome dynamics significantly correlated with coral species‐specific phenotypes. For example, bleaching and mortality inA. retusa both significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, whileP. lobata colonies 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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ABSTRACT Global climate change impacts marine ecosystems through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, less is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their tolerance to hypoxia. We conducted
in situ oxygen manipulations on a coral reef in Bahía Almirante on the Caribbean coast of Panama, which has previously experienced documented episodes of hypoxia. Naïve coral colonies (previously unexposed to hypoxia) ofSiderastrea siderea andAgaricia lamarcki were transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress or may represent opportunists exploiting host stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor.IMPORTANCE Marine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Though microbial symbioses can alleviate the effects of ecological stress, we do not yet understand the taxonomic or functional response of the coral microbiome to hypoxia. In this study, we experimentally lowered oxygen levels around
Siderastrea siderea andAgaricia lamarcki coloniesin situ to observe changes in the coral microbiome in response to deoxygenation. Our results show that hypoxia triggers a stochastic change of the microbiome overall, with some bacterial families changing deterministically after just 48 hours of exposure. These families represent an increase in anaerobic and opportunistic taxa in the microbiomes of both coral species. Thus, marine deoxygenation destabilizes the coral microbiome and increases bacterial opportunism. This work provides novel and fundamental knowledge of the microbial response in coral during hypoxia and may provide insight into holobiont function during stress. -
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Abstract Global climate change is altering coral reef ecosystems. Notably, marine heatwaves are producing widespread coral bleaching events that are increasing in frequency, with projections for annual bleaching events on reefs worldwide by mid‐century.
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Montipora capitata corals dominated by heat‐sensitiveCladocopium or heat‐tolerantDurusdinium Symbiodiniaceae at two reef sites.Despite fewer degree heating weeks in the first‐bleaching event relative to the second (7 vs. 10),
M. capitata bleaching severity was greater [bleached cover: ~70% (2014) vs. 50% (2015)] and environmental history (site effects) on coral phenotypes were more pronounced. Symbiodiniaceae affected bleaching responses, but immunity and antioxidant activity was similar in all corals, despite differences in bleaching phenotypes.We demonstrate that repeat bleaching triggers cellular responses that shift holobiont multivariate phenotypes. These perturbed multivariate phenotypes constitute physiological legacies, which set corals on trajectories (positive and/or negative) that influence future coral performance. Collectively, our data support the need for greater tracking of stress response in a multivariate context to better understand the biology and ecology of corals in the Anthropocene.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
Abstract Background Management actions that address local-scale stressors on coral reefs can rapidly improve water quality and reef ecosystem condition. In response to reef managers who need actionable thresholds for coastal runoff and dredging, we conducted a systematic review and meta-analysis of experimental studies that explore the effects of sediment on corals. We identified exposure levels that ‘adversely’ affect corals while accounting for sediment bearing (deposited vs. suspended), coral life-history stage, and species, thus providing empirically based estimates of stressor thresholds on vulnerable coral reefs. Methods We searched online databases and grey literature to obtain a list of potential studies, assess their eligibility, and critically appraise them for validity and risk of bias. Data were extracted from eligible studies and grouped by sediment bearing and coral response to identify thresholds in terms of the lowest exposure levels that induced an adverse physiological and/or lethal effect. Meta-regression estimated the dose–response relationship between exposure level and the magnitude of a coral’s response, with random-effects structures to estimate the proportion of variance explained by factors such as study and coral species. Review findings After critical appraisal of over 15,000 records, our systematic review of corals’ responses to sediment identified 86 studies to be included in meta-analyses (45 studies for deposited sediment and 42 studies for suspended sediment). The lowest sediment exposure levels that caused adverse effects in corals were well below the levels previously described as ‘normal’ on reefs: for deposited sediment, adverse effects occurred as low as 1 mg/cm 2 /day for larvae (limited settlement rates) and 4.9 mg/cm 2 /day for adults (tissue mortality); for suspended sediment, adverse effects occurred as low as 10 mg/L for juveniles (reduced growth rates) and 3.2 mg/L for adults (bleaching and tissue mortality). Corals take at least 10 times longer to experience tissue mortality from exposure to suspended sediment than to comparable concentrations of deposited sediment, though physiological changes manifest 10 times faster in response to suspended sediment than to deposited sediment. Threshold estimates derived from continuous response variables (magnitude of adverse effect) largely matched the lowest-observed adverse-effect levels from a summary of studies, or otherwise helped us to identify research gaps that should be addressed to better quantify the dose–response relationship between sediment exposure and coral health. Conclusions We compiled a global dataset that spans three oceans, over 140 coral species, decades of research, and a range of field- and lab-based approaches. Our review and meta-analysis inform the no-observed and lowest-observed adverse-effect levels (NOAEL, LOAEL) that are used in management consultations by U.S. federal agencies. In the absence of more location- or species-specific data to inform decisions, our results provide the best available information to protect vulnerable reef-building corals from sediment stress. Based on gaps and limitations identified by our review, we make recommendations to improve future studies and recommend future synthesis to disentangle the potentially synergistic effects of multiple coral-reef stressors.more » « less
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Abstract Background The importance of symbiosis has long been recognized on coral reefs, where the photosynthetic dinoflagellates of corals (Symbiodiniaceae) are the primary symbiont. Numerous studies have now shown that a diverse assemblage of prokaryotes also make-up part of the microbiome of corals. A subset of these prokaryotes is capable of fixing nitrogen, known as diazotrophs, and is also present in the microbiome of scleractinian corals where they have been shown to supplement the holobiont nitrogen budget. Here, an analysis of the microbiomes of 16 coral species collected from Australia, Curaçao, and Hawai’i using three different marker genes (16S rRNA, nif H, and ITS2) is presented. These data were used to examine the effects of biogeography, coral traits, and ecological life history characteristics on the composition and diversity of the microbiome in corals and their diazotrophic communities. Results The prokaryotic microbiome community composition (i.e., beta diversity) based on the 16S rRNA gene varied between sites and ecological life history characteristics, but coral morphology was the most significant factor affecting the microbiome of the corals studied. For 15 of the corals studied, only two species Pocillopora acuta and Seriotopora hystrix , both brooders, showed a weak relationship between the 16S rRNA gene community structure and the diazotrophic members of the microbiome using the nif H marker gene, suggesting that many corals support a microbiome with diazotrophic capabilities. The order Rhizobiales , a taxon that contains primarily diazotrophs, are common members of the coral microbiome and were eight times greater in relative abundances in Hawai’i compared to corals from either Curacao or Australia. However, for the diazotrophic component of the coral microbiome, only host species significantly influenced the composition and diversity of the community. Conclusions The roles and interactions between members of the coral holobiont are still not well understood, especially critical functions provided by the coral microbiome (e.g., nitrogen fixation), and the variation of these functions across species. The findings presented here show the significant effect of morphology, a coral “super trait,” on the overall community structure of the microbiome in corals and that there is a strong association of the diazotrophic community within the microbiome of corals. However, the underlying coral traits linking the effects of host species on diazotrophic communities remain unknown.more » « less
