Lauric Feugere
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
Adam Bates
Timothy Emagbetere
Emma Chapman
Linsey Malcolm
Kathleen Bulmer
Jörg Hardege
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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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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