scholarly journals Metabolome shift associated with thermal stress in coral holobionts

2020 ◽  
Author(s):  
Amanda Williams ◽  
Eric N. Chiles ◽  
Dennis Conetta ◽  
Jananan S. Pathmanathan ◽  
Phillip A. Cleves ◽  
...  
Keyword(s):  
Heat Stress ◽  
Thermal Stress ◽  
Coral Species ◽  
Related Function ◽  
Montipora Capitata ◽  
Algal Symbiont ◽  
Coral Holobiont ◽  
Algal Symbiosis ◽  
Coral Health ◽  
Global Threat

SummaryCoral reef systems are under global threat due to warming and acidifying oceans1. Understanding the response of the coral holobiont to environmental change is crucial to aid conservation efforts. The most pressing problem is “coral bleaching”, usually precipitated by prolonged thermal stress that disrupts the algal symbiosis sustaining the holobiont2,3. We used metabolomics to understand how the coral holobiont metabolome responds to heat stress with the goal of identifying diagnostic markers prior to bleaching onset. We studied the heat tolerant Montipora capitata and heat sensitive Pocillopora acuta coral species from the Hawaiian reef system in Kāne’ohe Bay, O’ahu. Untargeted LC-MS analysis uncovered both known and novel metabolites that accumulate during heat stress. Among those showing the highest differential accumulation were a variety of co-regulated dipeptides present in both species. The structures of four of these compounds were determined (Arginine-Glutamine, Lysine-Glutamine, Arginine-Valine, and Arginine-Alanine). These dipeptides also showed differential accumulation in symbiotic and aposymbiotic (alga free) individuals of the sea anemone model Aiptasia4, suggesting their animal provenance and algal symbiont related function. Our results identify a suite of metabolites associated with thermal stress that can be used to diagnose coral health in wild samples.

scholarly journals Metabolomic shifts associated with heat stress in coral holobionts

2021 ◽  
Vol 7 (1) ◽  
pp. eabd4210
Author(s):  
Amanda Williams ◽  
Eric N. Chiles ◽  
Dennis Conetta ◽  
Jananan S. Pathmanathan ◽  
Phillip A. Cleves ◽  
...  
Keyword(s):  
Heat Stress ◽  
Thermal Stress ◽  
Physiological Response ◽  
Metabolite Profiling ◽  
Coral Species ◽  
Diagnostic Markers ◽  
Evolutionary Origins ◽  
Coral Holobiont ◽  
Bleaching Response ◽  
Exaiptasia Pallida

Understanding the response of the coral holobiont to environmental change is crucial to inform conservation efforts. The most pressing problem is “coral bleaching,” usually precipitated by prolonged thermal stress. We used untargeted, polar metabolite profiling to investigate the physiological response of the coral species Montipora capitata and Pocillopora acuta to heat stress. Our goal was to identify diagnostic markers present early in the bleaching response. From the untargeted UHPLC-MS data, a variety of co-regulated dipeptides were found that have the highest differential accumulation in both species. The structures of four dipeptides were determined and showed differential accumulation in symbiotic and aposymbiotic (alga-free) populations of the sea anemone Aiptasia (Exaiptasia pallida), suggesting the deep evolutionary origins of these dipeptides and their involvement in symbiosis. These and other metabolites may be used as diagnostic markers for thermal stress in wild coral.

scholarly journals Variation in susceptibility among three Caribbean coral species and their algal symbionts indicates the threatened staghorn coral, Acropora cervicornis, is particularly susceptible to elevated nutrients and heat stress

2021 ◽  
Author(s):  
Ana M. Palacio-Castro ◽  
Caroline E. Dennison ◽  
Stephanie M. Rosales ◽  
Andrew C. Baker
Keyword(s):  
Heat Stress ◽  
Coral Species ◽  
Coral Cover ◽  
Photochemical Efficiency ◽  
Acropora Cervicornis ◽  
Nutrient Inputs ◽  
Algal Symbionts ◽  
Algal Symbiont ◽  
Orbicella Faveolata ◽  
Significant Mortality

Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal types were exposed to either ambient nutrients (A), elevated NH4 (N), or elevated NH4 + PO4 (N+P) at control temperatures (26 °C) for > 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%-100% mortality and photochemical efficiency (Fv/Fm) declines of 41-50%. In comparison, no mortality and lower Fv/Fm declines (11-20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in Fv/Fm (41-56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17-26% and 10-16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.

scholarly journals An algal symbiont (Breviolum psygmophilum) responds more strongly to chronic high temperatures than its facultatively symbiotic coral host (Astrangia poculata)

2021 ◽  
Author(s):  
Andrea N. Chan ◽  
Luis A. González-Guerrero ◽  
Roberto Iglesias-Prieto ◽  
Elizabeth M. Burmester ◽  
Randi D. Rotjan ◽  
...  
Keyword(s):  
Heat Stress ◽  
Thermal Stress ◽  
Stress Response ◽  
Coral Bleaching ◽  
Scleractinian Corals ◽  
Coral Host ◽  
Algal Symbionts ◽  
Algal Symbiont ◽  
Astrangia Poculata ◽  
And Control

AbstractScleractinian corals form the foundation of coral reefs by secreting skeletons of calcium carbonate. Their intracellular algal symbionts (Symbiodiniaceae) translocate a large proportion of photosynthate to the coral host, which is required to maintain high rates of calcification. Global warming is causing dissociation of coral host and algal symbiont, visibly presented as coral bleaching. Despite decades of study, the precise mechanisms of coral bleaching remain unknown. Separating the thermal stress response of the coral from the algal symbiont is key to understanding bleaching in tropical corals. The facultatively symbiotic northern star coral, Astrangia poculata, naturally occurs as both symbiotic and aposymbiotic (lacking algal symbionts) polyps – sometimes on the same coral colony. Thus, it is possible to separate the heat stress response of the coral host alone from the coral in symbiosis with its symbiont Breviolum psygmophilum. Using replicate symbiotic and aposymbiotic ramets of A. poculata, we conducted a chronic heat stress experiment to increase our understanding of the cellular mechanisms resulting in coral bleaching. Sustained high temperature stress resulted in photosynthetic dysfunction in B. psygmophilum, including a decline in maximum photosynthesis rate, maximum photochemical efficiency, and the absorbance peak of chlorophyll a. Interestingly, the metabolic rates of symbiotic and aposymbiotic corals were differentially impacted. RNAseq analysis revealed more differentially expressed genes between heat-stressed and control aposymbiotic colonies than heat-stressed and control symbiotic colonies. Notably, aposymbiotic colonies increased the expression of inflammation-associated genes such as nitric oxide synthases. Unexpectedly, the largest transcriptional response was observed between heat-stressed and control B. psygmophilum, including genes involved in photosynthesis, response to oxidative stress, and meiosis. Thus, it appears that the algal symbiont suppresses the immune response of the host, potentially increasing the vulnerability of the host to pathogens. The A. poculata-B. psygmophilum symbiosis provides a tractable model system for investigating thermal stress and immune challenge in scleractinian corals.

scholarly journals Heat stress destabilizes symbiotic nutrient cycling in corals

2021 ◽  
Vol 118 (5) ◽  
pp. e2022653118 ◽  
Author(s):  
Nils Rädecker ◽  
Claudia Pogoreutz ◽  
Hagen M. Gegner ◽  
Anny Cárdenas ◽  
Florian Roth ◽  
...  
Keyword(s):  
Heat Stress ◽  
Nutrient Cycling ◽  
Energy Demand ◽  
Metabolic Energy ◽  
Environmental Drivers ◽  
Coral Host ◽  
Stylophora Pistillata ◽  
Coral Holobiont ◽  
Algal Symbiosis ◽  
Energy Limitation

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral–algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral–algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral–algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.

scholarly journals Microplastics ingestion and heterotrophy in thermally stressed corals

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Jeremy B. Axworthy ◽  
Jacqueline L. Padilla-Gamiño
Keyword(s):  
Thermal Stress ◽  
Global Change ◽  
Coral Reefs ◽  
Coral Species ◽  
Pocillopora Damicornis ◽  
Montipora Capitata ◽  
Thermally Stressed

AbstractRising sea temperatures and increasing pollution threaten the fate of coral reefs and millions of people who depend on them. Some reef-building corals respond to thermal stress and subsequent bleaching with increases in heterotrophy, which may increase the risk of ingesting microplastics. Whether this heterotrophic plasticity affects microplastics ingestion or whether ingesting microplastics affects heterotrophic feeding in corals is unknown. To determine this, two coral species, Montipora capitata and Pocillopora damicornis, were exposed to ambient (~27 °C) and increased (~30 °C) temperature and then fed microplastics, Artemia nauplii, or both. Following thermal stress, both species significantly reduced feeding on Artemia but no significant decrease in microplastics ingestion was observed. Interestingly, P. damicornis only ingested microplastics when Artemia were also present, providing evidence that microplastics are not selectively ingested by this species and are only incidentally ingested when food is available. As the first study to examine microplastics ingestion following thermal stress in corals, our results highlight the variability in the risk of microplastics ingestion among species and the importance of considering multiple drivers to project how corals will be affected by global change.

scholarly journals Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling

2021 ◽  
Author(s):  
Nils Rädecker ◽  
Claudia Pogoreutz ◽  
Hagen M. Gegner ◽  
Anny Cárdenas ◽  
Gabriela Perna ◽  
...  
Keyword(s):  
Nitrogen Fixation ◽  
Heat Stress ◽  
Nutrient Cycling ◽  
Environmental Conditions ◽  
Nitrogen Availability ◽  
Coral Tissue ◽  
Stylophora Pistillata ◽  
Algal Symbionts ◽  
Coral Holobiont ◽  
Algal Symbiosis

AbstractEfficient nutrient cycling in the coral-algal symbiosis requires constant but limited nitrogen availability. Coral-associated diazotrophs, i.e., prokaryotes capable of fixing dinitrogen, may thus support productivity in a stable coral-algal symbiosis but could contribute to its breakdown when overstimulated. However, the effects of environmental conditions on diazotroph communities and their interaction with other members of the coral holobiont remain poorly understood. Here we assessed the effects of heat stress on diazotroph diversity and their contribution to holobiont nutrient cycling in the reef-building coral Stylophora pistillata from the central Red Sea. In a stable symbiotic state, we found that nitrogen fixation by coral-associated diazotrophs constitutes a source of nitrogen to the algal symbionts. Heat stress caused an increase in nitrogen fixation concomitant with a change in diazotroph communities. Yet, this additional fixed nitrogen was not assimilated by the coral tissue or the algal symbionts. We conclude that although diazotrophs may support coral holobiont functioning under low nitrogen availability, altered nutrient cycling during heat stress abates the dependence of the coral host and its algal symbionts on diazotroph-derived nitrogen. Consequently, the role of nitrogen fixation in the coral holobiont is strongly dependent on its nutritional status and varies dynamically with environmental conditions.

scholarly journals Community composition of coral associated Symbiodiniaceae is driven by fine scale environmental gradients

2021 ◽  
Author(s):  
Mariana Rocha de Souza ◽  
Carlo Caruso ◽  
Lupita Ruiz-Jones ◽  
Crawford Drury ◽  
Ruth D. Gates ◽  
...  
Keyword(s):  
Environmental Factors ◽  
Community Composition ◽  
Spatial Patterns ◽  
Coral Species ◽  
Multiple Scales ◽  
Environmental Gradients ◽  
Fine Scale ◽  
Montipora Capitata ◽  
Northern Site ◽  
Algal Symbiont

The survival of reef-building corals is dependent upon a symbiosis between the coral and the community of Symbiodiniaceae. Montipora capitata, one of the main reef building coral species in Hawaiʻi, is known to host a diversity of symbionts, but it remains unclear how they change spatially and whether environmental factors drive those changes. Here, we surveyed the Symbiodiniaceae community in 600 M. capitata colonies from 30 sites across Kāneʻohe Bay and tested for host specificity and environmental gradients driving spatial patterns of algal symbiont distribution. We found that the Symbiodiniaceae community differed markedly across sites, with M. capitata in the most open-ocean (northern) site hosting few or none of the genus Durusdinium, whereas individuals at other sites had a mix of Durusdinium and Cladocopium. Our study shows that the algal symbiont community composition responds to fine-scale differences in environmental gradients; depth and temperature variability were the most significant predictor of Symbiodiniaceae community, although environmental factors measured in the study explained only about 20% of observed variation. Identifying and mapping Symbiodiniaceae community distribution at multiple scales is an important step in advancing our understanding of algal symbiont diversity, distribution and evolution, and the potential responses of corals to future environmental change.

scholarly journals Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response of Montipora capitata following thermal pre-exposure and across multiple bleaching events

2020 ◽  
Author(s):  
Jenna Dilworth ◽  
Carlo Caruso ◽  
Valerie A. Kahkejian ◽  
Andrew C. Baker ◽  
Crawford Drury
Keyword(s):  
Thermal Stress ◽  
Community Composition ◽  
Photochemical Efficiency ◽  
Coral Host ◽  
Host Genotype ◽  
Reef Environment ◽  
Montipora Capitata ◽  
Algal Symbionts ◽  
Algal Symbiont ◽  
Photochemical Damage

AbstractAs sea surface temperatures increase worldwide due to climate change, coral bleaching events are becoming more frequent and severe, resulting in reef degradation. Leveraging the inherent ability of reef-building corals to acclimatize to thermal stress via pre-exposure to protective temperature treatments may become an important tool in improving the resilience of coral reefs to rapid environmental change. We investigated whether historical bleaching phenotype, coral host genotype, and exposure to protective temperature treatments would affect the response of the Hawaiian coral Montipora capitata to natural thermal stress. Fragments were collected from colonies that demonstrated different bleaching responses during the 2014-2015 event in Kāne’ohe Bay (O’ahu, Hawai’i) and exposed to four different artificial temperature pre-treatments (and a control at ambient temperature). After recovery, fragments experienced a natural thermal stress event either in laboratory conditions or their native reef environment. Response to thermal stress was quantified by measuring changes in the algal symbionts’ photochemical efficiency, community composition, and relative density. Historical bleaching phenotype was reflected in stable differences in symbiont community composition, with historically bleached corals containing only Cladocopium symbionts and historically non-bleached corals having mixed symbiont communities dominated by Durusdinium. Mixed-community corals lost more Cladocopium than Cladocopium-only corals during the natural thermal stress event, and preferentially recovered with Durusdinium. Laboratory pre-treatments exposed corals to more thermal stress than anticipated, causing photochemical damage that varied significantly by genotype. While none of the treatments had a protective effect, temperature variation during treatments had a significant detrimental effect on photochemical efficiency during the thermal stress event. These results show that acclimatization potential is affected by fine-scale differences in temperature regime, host genotype, and relatively stable differences in symbiont community composition that underpin historical bleaching phenotypes in M. capitata.

scholarly journals Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Viridiana Avila-Magaña ◽  
Bishoy Kamel ◽  
Michael DeSalvo ◽  
Kelly Gómez-Campo ◽  
Susana Enríquez ◽  
...  
Keyword(s):  
Gene Expression ◽  
Heat Stress ◽  
Coral Species ◽  
Complex Trait ◽  
Coral Host ◽  
Specific Expression ◽  
Coral Holobiont ◽  
Wide Range ◽  
Stress Experiment ◽  
Multiple Interactions

AbstractAs coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures.

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