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 ◽  
...  

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.

2021 ◽  
Author(s):  
Nils Rädecker ◽  
Claudia Pogoreutz ◽  
Hagen M. Gegner ◽  
Anny Cárdenas ◽  
Gabriela Perna ◽  
...  

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.


2020 ◽  
Author(s):  
Amanda Williams ◽  
Eric N. Chiles ◽  
Dennis Conetta ◽  
Jananan S. Pathmanathan ◽  
Phillip A. Cleves ◽  
...  

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.


2021 ◽  
Vol 118 (19) ◽  
pp. e2023298118
Author(s):  
Romain Savary ◽  
Daniel J. Barshis ◽  
Christian R. Voolstra ◽  
Anny Cárdenas ◽  
Nicolas R. Evensen ◽  
...  

Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean.


2020 ◽  
Vol 8 (3) ◽  
pp. 372
Author(s):  
Dalit Meron ◽  
Keren Maor-Landaw ◽  
Gal Eyal ◽  
Hila Elifantz ◽  
Ehud Banin ◽  
...  

The recognition of the microbiota complexity and their role in the evolution of their host is leading to the popularization of the holobiont concept. However, the coral holobiont (host and its microbiota) is still enigmatic and unclear. Here, we explore the complex relations between different holobiont members of a mesophotic coral Euphyllia paradivisa. We subjected two lines of the coral—with photosymbionts, and without photosymbionts (apo-symbiotic)—to increasing temperatures and to antibiotics. The different symbiotic states were characterized using transcriptomics, microbiology and physiology techniques. The bacterial community’s composition is dominated by bacteroidetes, alphaproteobacteria, and gammaproteobacteria, but is dependent upon the symbiont state, colony, temperature treatment, and antibiotic exposure. Overall, the most important parameter determining the response was whether the coral was a symbiont/apo-symbiotic, while the colony and bacterial composition were secondary factors. Enrichment Gene Ontology analysis of coral host’s differentially expressed genes demonstrated the cellular differences between symbiotic and apo-symbiotic samples. Our results demonstrate the significance of each component of the holobiont consortium and imply a coherent link between them, which dramatically impacts the molecular and cellular processes of the coral host, which possibly affect its fitness, particularly under environmental stress.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Viridiana Avila-Magaña ◽  
Bishoy Kamel ◽  
Michael DeSalvo ◽  
Kelly Gómez-Campo ◽  
Susana Enríquez ◽  
...  

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.


2020 ◽  
Vol 13 (1) ◽  
pp. 27
Author(s):  
Hatem Mahmoud ◽  
Ayman Ragab

The density of building blocks and insufficient greenery in cities tend to contribute dramatically not only to increased heat stress in the built environment but also to higher energy demand for cooling. Urban planners should, therefore, be conscious of their responsibility to reduce energy usage of buildings along with improving outdoor thermal efficiency. This study examines the impact of numerous proposed urban geometry cases on the thermal efficiency of outer spaces as well as the energy consumption of adjacent buildings under various climate change scenarios as representative concentration pathways (RCP) 4.5 and 8.5 climate projections for New Aswan city in 2035. The investigation was performed at one of the most underutilized outdoor spaces on the new campus of Aswan University in New Aswan city. The potential reduction of heat stress was investigated so as to improve the thermal comfort of the investigated outdoor spaces, as well as energy savings based on the proposed strategies. Accordingly, the most appropriate scenario to be adopted to cope with the inevitable climate change was identified. The proposed scenarios were divided into four categories of parameters. In the first category, shelters partially (25–50% and 75%) covering the streets were used. The second category proposed dividing the space parallel or perpendicular to the existing buildings. The third category was a hybrid scenario of the first and second categories. In the fourth category, a green cover of grass was added. A coupling evaluation was applied utilizing ENVI-met v4.2 and Design-Builder v4.5 to measure and improve the thermal efficiency of the outdoor space and reduce the cooling energy. The results demonstrated that it is better to cover outdoor spaces with 50% of the overall area than transform outdoor spaces into canyons.


2013 ◽  
Vol 10 (1) ◽  
pp. 83-109 ◽  
Author(s):  
P. Tremblay ◽  
M. Fine ◽  
J. F. Maguer ◽  
R. Grover ◽  
C. Ferrier-Pagès

Abstract. This study has examined the effect of an increased seawater pCO2 on the rates of photosynthesis and carbon translocation in the scleractinian coral species Stylophora pistillata using a new model based on 13C-labelling of the photosynthetic products. Symbiont photosynthesis contributes for a large part of the carbon acquisition in tropical coral species and is therefore an important process that may determine their survival under climate change scenarios. Nubbins of S. pistillata were maintained for six months under two pHs (8.1 and 7.2). Rates of photosynthesis and respiration of the symbiotic association and of isolated symbionts were assessed at each pH. The fate of 13C-photosynthates was then followed in the symbionts and the coral host for 48 h. Nubbins maintained at pH 7.2 presented a lower areal symbiont concentration, lower areal rates of gross photosynthesis, and lower carbon incorporation rates compared to nubbins maintained at pH 8.1, therefore suggesting that the total carbon acquisition was lower in this first set of nubbins. However, the total percentage of carbon translocated to the host, as well as the amount of carbon translocated per symbiont cell was significantly higher under pH 7.2 than under pH 8.1 (70% at pH 7.2 versus 60% at pH 8.1), so that the total amount of photosynthetic carbon received by the coral host was equivalent under both pHs (5.5 to 6.1 μg C cm−2 h−1). Although the carbon budget of the host was unchanged, symbionts acquired less carbon for their own needs (0.6 against 1.8 μg C cm−2 h−1), explaining the overall decrease in symbiont concentration at low pH. In the long-term, this decrease might have important consequences for the survival of corals under an acidification stress.


2019 ◽  
Vol 286 (1896) ◽  
pp. 20182444 ◽  
Author(s):  
Isabelle Taubner ◽  
Marian Y. Hu ◽  
Anton Eisenhauer ◽  
Markus Bleich

Light has been demonstrated to enhance calcification rates in hermatypic coral species. To date, it remains unresolved whether calcifying epithelia change their ion transport activity during illumination, and whether such a process is mediated by the endosymbiotic algae or can be controlled by the coral host itself. Using a modified Ussing chamber in combination with H + sensitive microelectrode measurements, the present work demonstrates that light triggers the generation of a skeleton positive potential of up to 0.9 mV in the hermatypic coral Stylophora pistillata . This potential is generated by a net flux of cations towards the skeleton and reaches its maximum at blue (450 nm) light. The effects of pharmacological inhibitors targeting photosynthesis 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) and anion transport 4,4'-diisothiocyano-2,2'-stilbenedisulfonic acid (DIDS) were investigated by pH microelectrode measurements in coral tissues demonstrating a rapid decrease in tissue pH under illumination. However, these inhibitors showed no effect on the electrophysiological light response of the coral host. By contrast, metabolic inhibition by cyanide and deoxyglucose reversibly inhibited the light-induced cation flux towards the skeleton. These results suggest that ion transport across coral epithelia is directly triggered by blue light, independent of photosynthetic activity of algal endosymbionts. Measurements of this very specific and quantifiable physiological response can provide parameters to identify photoreception mechanisms and will help to broaden our understanding of the mechanistic link between light stimulation and epithelial ion transport, potentially relevant for calcification in hermatypic corals.


2010 ◽  
Vol 19 (9) ◽  
pp. 1978-1990 ◽  
Author(s):  
RAECHEL A. LITTMAN ◽  
DAVID G. BOURNE ◽  
BETTE L. WILLIS

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