The heat shock response shows plasticity in embryonic lake whitefish (Coregonus clupeaformis) exposed to repeated thermal stress

Sessions, Katherine J.; Whitehouse, Lindy M.; Manzon, Lori A.; Boreham, Douglas R.; Somers, Christopher M.; Wilson, Joanna Y.; Manzon, Richard G.

doi:10.1016/j.jtherbio.2021.103036

Cited by 11 publications

(14 citation statements)

References 60 publications

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“…These inverted gene expression patterns under fluctuating as compared to constant thermal stress, might be related to energetic depletion as a result of the thermal cycles (Alfonso et al, 2020;Schaefer and Ryan, 2006). Repetition of heat stress also attenuated the response of heat shock proteins at the mRNA level in lake whitefish (Coregonus clupeaformis) embryos (Sessions et al, 2021;Whitehouse et al, 2017). However, HSP70 protein levels remained upregulated by heat stress in our experiment.…”

Section: Fluctuating High Temperatures Induce a Stress Response In Ze...mentioning

confidence: 47%

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

Feugere

Scott

Rodriguez-Barucg

et al. 2021

Journal of Thermal Biology

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Section: Fluctuating High Temperatures Induce a Stress Response In Ze...mentioning

confidence: 47%

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

Feugere

Scott

Rodriguez-Barucg

et al. 2021

Journal of Thermal Biology

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“…The type of stimulus also matters: single and repeated periods of heat can induce different gene expression patterns leading to distinct behavioural stress responses (6). Repeated thermal conditioning can impair the ability to restore homeostasis (7) and alter the response to subsequent heat stress by attenuating the corticosteroid (8) and heat shock (9, 10) pathways. Furthermore, there is a growing concern about the response of fish embryos to heat due to their narrower thermal tolerance (11, 12), marking early development as a vulnerable “bottleneck” stage (13) when it comes to thermal stress.…”

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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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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“…The up-regulation of heat shock protein (HSPs) transcripts and cortisol confirmed that repeated heat stress induced a (cellular and heat) stress response independent of faster development ( 42 , 43 ). However, the induction of HSP70 found at 1 dpf ( 16 ) was no longer present in 4-dpf larvae having experienced 4 days of repeated heat peaks, which suggests either attenuation of the heat shock response ( 9 , 10 ) or habituation to higher temperatures. One limitation of our study is that we only measured protein levels of HSP70, but a more comprehensive picture could be obtained by analyzing other heat-responsive chaperone proteins.…”

Section: Discussionmentioning

confidence: 98%

“…The type of stimulus also matters: single and repeated periods of heat can induce different gene expression patterns leading to distinct behavioral stress responses ( 6 ). Repeated thermal conditioning can impair the ability to restore homeostasis ( 7 ) and alter the response to subsequent heat stress by attenuating the corticosteroid ( 8 ) and heat shock ( 9 , 10 ) pathways. Furthermore, there is a growing concern about the response of fish embryos to heat due to their narrower thermal tolerance ( 11 , 12 ), marking early development as a vulnerable “bottleneck” stage ( 13 ) when it comes to thermal stress.…”

Section: Introductionmentioning

confidence: 99%

Heat induces multiomic and phenotypic stress propagation in zebrafish embryos

et al. 2023

View full text Add to dashboard Cite

Heat alters biology from molecular to ecological levels, but may also have unknown indirect effects. This includes the 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 multiomic 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 slowdown in concert with reduced responses to novel stimuli. Metabolomes of the media of heat treated vs. untreated embryos revealed candidate stress metabolites including sulfur-containing compounds and lipids. These stress metabolites elicited transcriptomic changes in naive receivers related to immune response, extracellular signaling, glycosaminoglycan/keratan sulfate, 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 signaling. Our results prove the concept of indirect heat-induced stress propagation toward naive receivers, inducing phenotypes comparable with those resulting from direct heat exposure, but utilizing distinct molecular pathways. Group-exposing a nonlaboratory 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 the 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.

show abstract

The heat shock response shows plasticity in embryonic lake whitefish (Coregonus clupeaformis) exposed to repeated thermal stress

Cited by 11 publications

References 60 publications

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

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

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

Heat induces multiomic and phenotypic stress propagation in zebrafish embryos

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