Thermal stress induces a positive phenotypic and molecular feedback loop in zebrafish embryos

Feugere, Lauric; Scott, Victoria F.; Rodriguez-Barucg, Quentin; Beltrán-Álvarez, Pedro; Valero, Katharina C. Wollenberg

doi:10.1016/j.jtherbio.2021.103114

Cited by 13 publications

(29 citation statements)

References 104 publications

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“…Previous studies have focused mostly on cues released upon biotic factors such as injury (14) or disturbance (15). We have recently proposed that abiotic stress such as heat or low pH likewise elicits the release of olfactory cues, which we termed “stress metabolites” (16, 17). We found these cues to elicit similar phenotypic responses as heat stress itself in naive receivers, which are the characteristics of a positive feedback loop (16).…”

Section: Introductionmentioning

confidence: 99%

“…We have recently proposed that abiotic stress such as heat or low pH likewise elicits the release of olfactory cues, which we termed “stress metabolites” (16, 17). We found these cues to elicit similar phenotypic responses as heat stress itself in naive receivers, which are the characteristics of a positive feedback loop (16). To date, only a few studies have shown that animals communicate to each other upon abiotic stress, such as heat and low pH (17, 18).…”

Section: Introductionmentioning

confidence: 99%

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Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Feugere

Bates

Emagbetere

et al. 2022

Preprint

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Heat alters biology from molecular to ecological levels, but may also have unknown indirect effects. This includes the novel concept that animals exposed to abiotic stress can induce stress in naive receivers. Here, we provide a comprehensive picture of the molecular signatures of this process, by integrating multi-omic and phenotypic data. In individual zebrafish embryos, repeated heat peaks elicited both a molecular response and a burst of accelerated growth followed by a growth slow-down in concert with reduced responses to novel stimuli. Metabolomes of the media of heat treated vs. untreated embryos revealed candidate stress metabolites including sulphur-containing compounds and lipids. These stress metabolites elicited transcriptomic changes in naive receivers related to immune response, extracellular signalling, glycosaminoglycan/keratan sulphate, and lipid metabolism. Consequently, non heat-exposed receivers (exposed to stress metabolites only) experienced accelerated catch-up growth in concert with reduced swimming performance. The combination of heat and stress metabolites accelerated development the most, mediated by apelin signalling. Our results prove the concept of indirect heat-induced stress propagation towards naive receivers, inducing phenotypes comparable to those resulting from direct heat exposure, but utilising distinct molecular pathways. Group-exposing a non-laboratory zebrafish line, we independently confirm that the glycosaminoglycan biosynthesis-related gene chs1, and the mucus glycoprotein gene prg4a, functionally connected to the candidate stress metabolite classes sugars and phosphocholine, are differentially expressed in receivers. This hints at production of Schreckstoff-like cues in receivers, leading to further stress propagation within groups, which may have ecological and animal welfare implications for aquatic populations in a changing climate.Significance StatementAquatic animals utilise chemicals to mediate adaptive behaviours. For instance, predated fish release chemical cues that elicit antipredatory responses in naive receivers. But whether abiotic factors such as heat likewise alter chemical communication has received little focus. Here, we uncover a novel dimension of chemical communication — heat-stressed donors can induce stress in naive receivers. We show that heat activates molecular stress responses, leading to the release of distinct stress metabolite classes into the environment. These stress metabolites alter the transcriptome of receivers, resulting in faster development and hypoactivity. Heat combined with stress metabolites had the largest effect, highlighting that abiotic stress, experienced both directly and indirectly, can alter chemical communication and affect embryonic development.Graphical AbstractHighlightsWe elucidate the mechanism for a novel dimension of the heat stress response — chemical communication from heat-stressed donors that induces stress in naive receivers — constituting a positive feedback loopRepeated heat stress induces a cellular and cortisol stress response and alters the phenotype of zebrafish embryosHeat-stressed embryos release stress metabolites enriched in lipids and sulphur-containing organo-oxygen compoundsIn combination, heat and stress metabolites induced 47% distinct differentially expressed genes, with many related to organ developmentThese stress metabolites alter the transcriptome and induce both faster development and hypoactivity in naive receivers, a similar response to that of heat stress itself

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Feugere

Bates

Emagbetere

et al. 2022

Preprint

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“…Whereas temperatures ranging from 26–28°C are often considered constant ‘optimal’ temperatures for laboratory zebrafish (e.g. promoting growth, fecundity, and immune responses [ 33 , 34 ]), 22–32°C represents the maximum range of temperatures under which zebrafish develop normally, representing the extreme developmental thermal boundary beyond which high levels of mortality, deformation and thermal stress occur [ 35 , 36 ]. Yet, during reproductive season in natural habitats, temperatures tend to vary from approximately 23–31°C [ 34 ].…”

Section: Methodsmentioning

confidence: 99%

“…R. Soc. B 289: 20220751 [35,36]. Yet, during reproductive season in natural habitats, temperatures tend to vary from approximately 23-31°C [34].…”

Section: Methods (A) Parental Fish Rearing and Breedingmentioning

confidence: 99%

Differential reproductive plasticity under thermal variability in a freshwater fish ( Danio rerio )

et al. 2022

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Human-driven increases in global mean temperatures are associated with concomitant increases in thermal variability. Yet, few studies have explored the impacts of thermal variability on fitness-related traits, limiting our ability to predict how organisms will respond to dynamic thermal changes. Among the myriad organismal responses to thermal variability, one of the most proximate to fitness—and, thus, a population's ability to persist—is reproduction. Here, we examine how a model freshwater fish ( Danio rerio ) responds to diel thermal fluctuations that span the species's viable developmental range of temperatures. We specifically investigate reproductive performance metrics including spawning success, fecundity, egg provisioning and sperm concentration. Notably, we apply thermal variability treatments during two ontogenetic timepoints to disentangle the relative effects of developmental plasticity and reversible acclimation. We found evidence of direct, negative effects of thermal variability during later ontogenetic stages on reproductive performance metrics. We also found complex interactive effects of early and late-life exposure to thermal variability, with evidence of beneficial acclimation of spawning success and modification of the relationship between fecundity and egg provisioning. Our findings illuminate the plastic life-history modifications that fish may undergo as their thermal environments become increasingly variable.

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“…A directionally similar response to pH drop and to the stress metabolites it induces shows that pH drop can have indirect effects through stress propagation (Figure 1A), by which stressed animals directly experiencing environmental stressors negatively influence fitness-relevant behaviours of community members. The stress propagation toward naive conspecific individuals might constitute a "positive stress feedback loop" (Feugere et al, 2021). This was first observed by Hazlett (1985) after freshwater crayfish exposed to water conditioned with heat-stressed conspecifics displayed increased alertness, after returning the conditioned water to normal temperature.…”

Section: Indirect Effects Of Ph Drop On Recipients' Behaviour Through Stress Chemical Communicationmentioning

confidence: 99%

Behavioural Stress Propagation in Benthic Invertebrates Caused by Acute pH Drop-Induced Metabolites

Feugere

et al. 2021

Front. Mar. Sci.

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Studies on pH stress in marine animals typically focus on direct or species-specific aspects. We here test the hypothesis that a drop to pH = 7.6 indirectly affects the intra- and interspecific interactions of benthic invertebrates by means of chemical communication. We recorded fitness-relevant behaviours of small hermit crabs Diogenes pugilator, green shore crabs Carcinus maenas, and harbour ragworms Hediste diversicolor in response to short-term pH drop, and to putative stress metabolites released by conspecifics or gilt-head sea bream Sparus aurata during 30 min of acute pH drop. Not only did acute pH drop itself impair time to find a food cue in small hermit crabs and burrowing in harbour ragworms, but similar effects were observed under exposure to pH drop-induced stress metabolites. Stress metabolites from S. aurata, but not its regular control metabolites, also induced avoidance responses in all recipient species. Here, we confirm that a short-term abrupt pH drop, an abiotic stressor, has the capacity to trigger the release of metabolites which induce behavioural responses in conspecific and heterospecific individuals, which can be interpreted as a behavioural cost. Our findings that stress responses can be indirectly propagated through means of chemical communication warrant further research to confirm the effect size of the behavioural impairments caused by stress metabolites and to characterise their chemical nature.

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Thermal stress induces a positive phenotypic and molecular feedback loop in zebrafish embryos

Cited by 13 publications

References 104 publications

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

Differential reproductive plasticity under thermal variability in a freshwater fish ( Danio rerio )

Behavioural Stress Propagation in Benthic Invertebrates Caused by Acute pH Drop-Induced Metabolites

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