Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis (original) (raw)
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bioRxiv (Cold Spring Harbor Laboratory), 2023
Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was to a large extent concealed by body shrinkage of the starving animals, resulting in what could be referred to as 'invisible' bleaching. Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in our warming oceans.
Scientific Reports, 2022
Understanding the factors and processes that shape intra-specific sensitivity to heat stress is fundamental to better predicting the vulnerability of benthic species to climate change. Here, we investigate the response of a habitat-forming Mediterranean octocoral, the red gorgonian Paramuricea clavata (Risso, 1826) to thermal stress at multiple biological and geographical scales. Samples from eleven P. clavata populations inhabiting four localities separated by hundreds to more than 1500 km of coast and with contrasting thermal histories were exposed to a critical temperature threshold (25 °C) in a common garden experiment in aquaria. Ten of the 11 populations lacked thermotolerance to the experimental conditions provided (25 days at 25 °C), with 100% or almost 100% colony mortality by the end of the experiment. Furthermore, we found no significant association between local average thermal regimes nor recent thermal history (i.e., local water temperatures in the 3 months prior to the experiment) and population thermotolerance. Overall, our results suggest that local adaptation and/or acclimation to warmer conditions have a limited role in the response of P. clavata to thermal stress. The study also confirms the sensitivity of this species to warm temperatures across its distributional range and questions its adaptive capacity under ocean warming conditions. However, important inter-individual variation in thermotolerance was found within populations, particularly those exposed to the most severe prior marine heatwaves. These observations suggest that P. clavata could harbor adaptive potential to future warming acting on standing genetic variation (i.e., divergent selection) and/or environmentally-induced phenotypic variation (i.e., intra-and/or intergenerational plasticity). Ocean warming is imposing increasing stress on marine ecosystems by exposing marine species to extreme temperatures that may exceed their thermal limits 1. However, populations and individuals of the same species exhibit contrasting responses to warming across different spatio-temporal scales 2-4. This intra-specific variability hinders our understanding of species vulnerability to climate change, and therefore, of any potential derived effect that may cascade up to the community or ecosystem level. The capacity of sessile marine species to persist in the face of climate change is highly influenced by their thermal tolerances, which tend to reflect the environment in which they are found 5. Accordingly, much research
PLoS ONE, 2012
Background: The knowledge about the capacity of organisms' early life stages to adapt to elevated temperatures is very limited but crucial to understand how marine biota will respond to global warming. Here we provide a comprehensive and integrated view of biological responses to future warming during the early ontogeny of a keystone invertebrate, the squid Loligo vulgaris. Methodology/Principal Findings: Recently-spawned egg masses were collected and reared until hatching at present day and projected near future (+2uC) temperatures, to investigate the ability of early stages to undergo thermal acclimation, namely phenotypic altering of morphological, behavioural, biochemical and physiological features. Our findings showed that under the projected near-future warming, the abiotic conditions inside the eggs promoted metabolic suppression, which was followed by premature hatching. Concomitantly, the less developed newborns showed greater incidence of malformations. After hatching, the metabolic burst associated with the transition from an encapsulated embryo to a planktonic stage increased linearly with temperature. However, the greater exposure to environmental stress by the hatchlings seemed to be compensated by physiological mechanisms that reduce the negative effects on fitness. Heat shock proteins (HSP70/HSC70) and antioxidant enzymes activities constituted an integrated stress response to ocean warming in hatchlings (but not in embryos). Conclusions/Significance: The stressful abiotic conditions inside eggs are expected to be aggravated under the projected near-future ocean warming, with deleterious effects on embryo survival and growth. Greater feeding challenges and the lower thermal tolerance limits of the hatchlings are strictly connected to high metabolic demands associated with the planktonic life strategy. Yet, we found some evidence that, in the future, the early stages might support higher energy demands by adjusting some cellular functional properties to increase their thermal tolerance windows.
Sub-littoral and supra-littoral amphipods respond differently to acute thermal stress
Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 2010
Thermal tolerance was determined in two closely related amphipod species from contrasting environments (sub-littoral and supra-littoral zones of the sea) using HSP expression and the activity of antioxidant enzymes. The levels of HSP70 and small HSPs present in untreated control animals were higher in the supra-littoral Orchestia gammarellus than in the sub-littoral Gammarus oceanicus. Under the acute thermal stress, HSP levels increased less strongly in O. gammarellus than in G. oceanicus. Activities of antioxidant enzymes peroxidase, catalase and glutathione S-transferase, were more pronounced in the supra-littoral O. gammarellus then in the sub-littoral G. oceanicus. We conclude that the environmental temperature regime modifies key cellular defense mechanisms in amphipods. Higher levels of constitutive HSP synthesis and higher levels of antioxidant enzymes in the supra-littoral species likely reflects adaptation to this highly thermally variable environment.
Marine Ecology Progress Series, 2012
While, in lower latitudes, population-level differences in heat tolerance are linked to temperature variability, in the Southern Ocean remarkably stable year-round temperatures prevail. Temporal variation in the physiology of Antarctic ectotherms is therefore thought to be driven by the intense seasonality in primary productivity. Here we tested for differences in the acute upper temperature limits (lethal and activity) of 2 Antarctic marine invertebrates (the omnivorous starfish Odontaster validus and the filter-feeding clam Laternula elliptica) across latitude, seasons and years. Acute thermal responses in the starfish (righting and feeding) and clam (burrowing) differed between populations collected at 77°S (McMurdo Sound) and 67°S (Marguerite Bay). Both species displayed significantly higher temperature performance at 67°S, where seawater can reach a maximum of +1.8°C in summer versus −0.5°C at 77°S, showing that even the narrow spatial and temporal variation in environmental temperature in Antarctica is biologically meaningful to these stenothermal invertebrates. Temporal comparisons of heat tolerance also demonstrated seasonal differences in acute upper limits for survival that were consistent with physiological acclimatisation: lethal limits were lower in winter than summer and higher in warm years than cool years. However, clams had greater inter-annual variation of temperature limits than was observed for starfish, suggesting that variation in food availability is also an important factor, particularly for primary consumers. Teasing out the interaction of multiple factors on thermal tolerance will be important for refining species-specific predictions of climate change impacts.
Biology Letters
Under global warming scenarios, rising temperatures can constitute heat stress to which species may respond differentially. Within a described species, knowledge on cryptic diversity is of further relevance, as different lineages/cryptic species may respond differentially to environmental change. The Brachionus calyciflorus species complex (Rotifera), which was recently described using integrative taxonomy, is an essential component of aquatic ecosystems. Here, we tested the hypothesis that these (formerly cryptic) species differ in their heat tolerance. We assigned 47 clones with nuclear ITS1 (nuITS1) and mitochondrial COI (mtCOI) markers to evolutionary lineages, now named B. calyciflorus sensu stricto (s.s.) and B. fernandoi . We selected 15 representative clones and assessed their heat tolerance as a bi-dimensional phenotypic trait affected by both the intensity and duration of heat stress. We found two distinct groups, with B. calyciflorus s.s. clones having higher heat toleran...
Conservation Physiology, 2020
Widespread declines in the body size of aquatic ectotherms have been attributed to the poorer ability of older, larger individuals to tolerate high temperature. Here, using the thermal death time curve framework, we investigate the relationship between temperature tolerance and size/age by measuring the change in heat tolerance of the keystone zooplankton species Daphnia magna across a range of temperature intensities (and hence exposures of varying duration) among individuals that differed up to 3-fold in size and thus varied in age also. Across the gradient of exposure temperatures, younger, smaller individuals were more tolerant than older, larger individuals. This suggests that the young and the small may be better equipped to withstand temperature challenges that are both intense/brief and more moderate/prolonged. Our study generalizes results obtained from more acute tolerance assays, providing physiological evidence consistent with the observed reductions in ectotherm body si...
Ecology and Evolution, 2017
Global warming has been changing the phenology, abundance, and distribution of many taxa in marine and terrestrial ecosystems (e.g., Falkowski, 2012; Thackeray, Jones, & Maberly, 2008) and ultimately affects all living taxa on earth. The immediate outcomes of climate change include ocean acidification, ocean warming, sea level rise (and subsequent changes in ocean circulation), and decrease in salinity (Houghton et al., 2001). For the potentially particularly affected benthic marine invertebrates, very little data exist and more empirical data are urgently needed in order to better understand possible changes in marine benthic ecosystems (Chen, 2008; Törnroos et al., 2014). Animal populations may respond to shifting conditions in different ways, for example, expanding their ecological niche and/or by moving to a new habitat (Hinder et al., 2014). How such demographic processes will develop in the future has become a crucial question in many areas of ecological research. Habitat suitability models, which aim to predict how species ranges might change, are a theoretical means to find answers (e.g., Paknia & Schierwater, 2015; Törnroos et al., 2014). On the other side, empirical measures may include the use of sensitive biomarkers in long-term monitoring studies and promise to be more sensitive and possibly also more reliable (cf.
Proceedings. Biological sciences, 2018
Corals and their endosymbiotic dinoflagellates of the genus have a fragile relationship that breaks down under heat stress, an event known as bleaching. However, many coral species have adapted to high temperature environments such as the Red Sea (RS). To investigate mechanisms underlying temperature adaptation in zooxanthellate cnidarians we compared transcriptome- and proteome-wide heat stress response (24 h at 32°C) of three strains of the model organism from regions with differing temperature profiles; North Carolina (CC7), Hawaii (H2) and the RS. Correlations between transcript and protein levels were generally low but inter-strain comparisons highlighted a common core cnidarian response to heat stress, including protein folding and oxidative stress pathways. RS anemones showed the strongest increase in antioxidant gene expression and exhibited significantly lower reactive oxygen species (ROS) levels However, comparisons of antioxidant gene and protein expression between strain...