scholarly journals Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

Author(s):  
Christian Voolstra ◽  
Jacob Valenzuela ◽  
Serdar Turkarslan ◽  
Anny Cardenas ◽  
Benjamin Hume ◽  
...  

Abstract Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5°C above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during re-colonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus Central Red Sea (CRS) Stylophora pistillata corals using the Coral Bleaching Automated Stress System (CBASS) to run a series of standardized acute thermal stress assays. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7°C above MMM). However, absolute thermal thresholds of CRS corals were on average 3°C above those of GoA corals. To explore the mechanistic underpinnings, we determined gene expression response and microbiome dynamics of coral holobiont compartments. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals versus a remarkably muted response in corals from the CRS. This pattern was recapitulated in the algal symbionts that showed site-specific genetic differentiation. Concomitant to this, a subset of coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression, i.e. front-loading, in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed consistent assemblages, indicating distinct microbial response patterns. Our work demonstrates distinct patterns underlying thermal tolerance across spatial scales, even for the same species and ocean basin. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that affect the response of coral populations to ocean warming.

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.


2021 ◽  
Author(s):  
Christian R. Voolstra ◽  
Jacob J. Valenzuela ◽  
Serdar Turkarslan ◽  
Anny Cárdenas ◽  
Benjamin C. C. Hume ◽  
...  

2021 ◽  
Vol 12 ◽  
Author(s):  
Angélica Jaramillo ◽  
Luis E. Castañeda

The gut microbiota can contribute to host physiology leading to an increase of resistance to abiotic stress conditions. For instance, temperature has profound effects on ectotherms, and the role of the gut microbiota on the thermal tolerance of ectotherms is a matter of recent research. However, most of these studies have been focused on single static temperatures instead of evaluating thermal tolerance in a wide range of stressful temperatures. Additionally, there is evidence supporting that the gut microbiota is sensitive to environmental temperature, which induces changes in its composition and diversity. These studies have evaluated the effects of thermal acclimation (>2 weeks) on the gut microbiota, but we know little about the impact of transient thermal stress on the composition and diversity of the gut microbiota. Thus, we investigated the role of the gut microbiota on the heat tolerance of Drosophila subobscura by measuring the heat tolerance of conventional and axenic flies exposed to different heat stressful temperatures (35, 36, 37, and 38°C) and estimating the heat tolerance landscape for both microbiota treatments. Conventional flies exposed to mild heat conditions exhibited higher thermal tolerance than axenic flies, whereas at higher stressful temperatures there were no differences between axenic and conventional flies. We also assessed the impact of transient heat stress on the taxonomical abundance, diversity, and community structure of the gut microbiota, comparing non-stressed flies (exposed to 21°C) and heat-stressed flies (exposed to 34°C) from both sexes. Bacterial diversity indices, bacterial abundances, and community structure changed between non-stressed and heat-stressed flies, and this response was sex-dependent. In general, our findings provide evidence that the gut microbiota influences heat tolerance and that heat stress modifies the gut microbiota at the taxonomical and structural levels. These results demonstrate that the gut microbiota contributes to heat tolerance and is also highly sensitive to transient heat stress, which could have important consequences on host fitness, population risk extinction, and the vulnerability of ectotherms to current and future climatic conditions.


2020 ◽  
Vol 287 (1922) ◽  
pp. 20193001 ◽  
Author(s):  
Marlene Wesselmann ◽  
Andrea Anton ◽  
Carlos M. Duarte ◽  
Iris E. Hendriks ◽  
Susana Agustí ◽  
...  

Exotic species often face new environmental conditions that are different from those that they are adapted to. The tropical seagrass Halophila stipulacea is a Lessepsian migrant that colonized the Mediterranean Sea around 100 years ago, where at present the minimum seawater temperature is cooler than in its native range in the Red Sea. Here, we tested if the temperature range in which H. stipulacea can exist is conserved within the species or if the exotic populations have shifted their thermal breadth and optimum due to the cooler conditions in the Mediterranean. We did so by comparing the thermal niche (e.g. optimal temperatures, and upper and lower thermal limits) of native (Saudi Arabia in the Red Sea) and exotic (Greece and Cyprus in the Mediterranean Sea) populations of H. stipulacea . We exposed plants to 12 temperature treatments ranging from 8 to 40°C for 7 days. At the end of the incubation period, we measured survival, rhizome elongation, shoot recruitment, net population growth and metabolic rates. Upper and lower lethal thermal thresholds (indicated by 50% plant mortality) were conserved across populations, but minimum and optimal temperatures for growth and oxygen production were lower for Mediterranean populations than for the Red Sea one. The displacement of the thermal niche of exotic populations towards the colder Mediterranean Sea regime could have occurred within 175 clonal generations.


2017 ◽  
Vol 4 (5) ◽  
pp. 170038 ◽  
Author(s):  
Thomas Krueger ◽  
Noa Horwitz ◽  
Julia Bodin ◽  
Maria-Evangelia Giovani ◽  
Stéphane Escrig ◽  
...  

Coral reefs are currently experiencing substantial ecological impoverishment as a result of anthropogenic stressors, and the majority of reefs are facing immediate risk. Increasing ocean surface temperatures induce frequent coral mass bleaching events—the breakdown of the nutritional photo-symbiosis with intracellular algae (genus: Symbiodinium ). Here, we report that Stylophora pistillata from a highly diverse reef in the Gulf of Aqaba showed no signs of bleaching despite spending 1.5 months at 1–2°C above their long-term summer maximum (amounting to 11 degree heating weeks) and a seawater pH of 7.8. Instead, their symbiotic dinoflagellates exhibited improved photochemistry, higher pigmentation and a doubling in net oxygen production, leading to a 51% increase in primary productivity. Nanoscale secondary ion mass spectrometry imaging revealed subtle cellular-level shifts in carbon and nitrogen metabolism under elevated temperatures, but overall host and symbiont biomass proxies were not significantly affected. Now living well below their thermal threshold in the Gulf of Aqaba, these corals have been evolutionarily selected for heat tolerance during their migration through the warm Southern Red Sea after the last ice age. This may allow them to withstand future warming for a longer period of time, provided that successful environmental conservation measures are enacted across national boundaries in the region.


2019 ◽  
Vol 286 (1898) ◽  
pp. 20190235 ◽  
Author(s):  
Thomas M. DeCarlo ◽  
Hugo B. Harrison ◽  
Laura Gajdzik ◽  
Diego Alaguarda ◽  
Riccardo Rodolfo-Metalpa ◽  
...  

Reef-building corals typically live close to the upper limits of their thermal tolerance and even small increases in summer water temperatures can lead to bleaching and mortality. Projections of coral reef futures based on forecasts of ocean temperatures indicate that by the end of this century, corals will experience their current thermal thresholds annually, which would lead to the widespread devastation of coral reef ecosystems. Here, we use skeletal cores of long-lived Porites corals collected from 14 reefs across the northern Great Barrier Reef, the Coral Sea, and New Caledonia to evaluate changes in their sensitivity to heat stress since 1815. High-density ‘stress bands’—indicative of past bleaching—first appear during a strong pre-industrial El Niño event in 1877 but become significantly more frequent in the late twentieth and early twenty-first centuries in accordance with rising temperatures from anthropogenic global warming. However, the proportion of cores with stress bands declines following successive bleaching events in the twenty-first century despite increasing exposure to heat stress. Our findings demonstrate an increase in the thermal tolerance of reef-building corals and offer a glimmer of hope that at least some coral species can acclimatize fast enough to keep pace with global warming.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3802
Author(s):  
Arjen Tilstra ◽  
Tim Wijgerde ◽  
Francisco Dini-Andreote ◽  
Britas Klemens Eriksson ◽  
Joana Falcão Salles ◽  
...  

Recent research suggests that prior exposure of several months to elevated irradiance induces enhanced thermal tolerance in scleractinian corals. While this tolerance has been reported at the species level, individual coral colonies may react differently due to individual variability in thermal tolerance. As thermal anomalies are predicted to become common in the upcoming future, intraspecific variation may be key to the survival of coral populations. In order to study light-history based thermal stress responses on individual colonies, we developed a preliminary microcosm experiment where three randomly chosen, aquacultured colonies of the model coral Stylophora pistillata were exposed to two irradiance treatments (200 and 400 μmol photons m−2 s−1) for 31 days, followed by artificially induced heat stress (∼33.4 °C). We found different responses to occur at both the intraspecific and the intracolonial levels, as indicated by either equal, less severe, delayed, and/or even non-necrotic responses of corals previously exposed to the irradiance of 400 compared to 200 μmol photons m−2 s−1. In addition, all individual colonies revealed light-enhanced calcification. Finally, elevated irradiance resulted in a lower chlorophyll a concentration in one colony compared to the control treatment, and the same colony displayed more rapid bleaching compared to the other ones. Taken together, this study highlights the potential importance of intra-individual variability in physiological responses of scleractinian corals and provides recommendations for improving methodological designs for future studies.


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