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Heat induces multiomic and phenotypic stress propagation in zebrafish embryos

Feugere, Lauric; Bates, Adam; Emagbetere, Timothy; Chapman, Emma; Malcolm, Linsey; Bulmer, Kathleen; Hardege, Jörg; Beltran-Alvarez, Pedro; Wollenberg Valero, Katharina C.

Authors

Lauric Feugere

Adam Bates

Timothy Emagbetere

Emma Chapman

Linsey Malcolm

Kathleen Bulmer

Jörg Hardege

Profile image of Pedro Beltran-Alvarez

Dr Pedro Beltran-Alvarez P.Beltran-Alvarez@hull.ac.uk
Senior Lecturer in Health and Climate Change and Programme co-Director of the MSc Health and Climate Change

Katharina C. Wollenberg Valero



Abstract

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.

Citation

Feugere, L., Bates, A., Emagbetere, T., Chapman, E., Malcolm, L., Bulmer, K., Hardege, J., Beltran-Alvarez, P., & Wollenberg Valero, K. C. (2023). Heat induces multiomic and phenotypic stress propagation in zebrafish embryos. PNAS Nexus, 2(5), Article pgad137. https://doi.org/10.1093/pnasnexus/pgad137

Journal Article Type Article
Acceptance Date Apr 11, 2023
Online Publication Date May 23, 2023
Publication Date May 1, 2023
Deposit Date May 10, 2023
Publicly Available Date May 26, 2023
Journal PNAS Nexus
Print ISSN 2752-6542
Electronic ISSN 2752-6542
Publisher National Academy of Sciences
Peer Reviewed Peer Reviewed
Volume 2
Issue 5
Article Number pgad137
DOI https://doi.org/10.1093/pnasnexus/pgad137
Keywords Stress cues; Stress propagation; Stress response; Thermal stress; Multiomics
Public URL https://hull-repository.worktribe.com/output/4288169

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Publisher Licence URL
http://creativecommons.org/licenses/by/4.0

Copyright Statement
© The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. This is an Open Access article
distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits
unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.




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