Metabolomic and phenotypic effects of ocean acidification on cuttlefish differ across early life stages

Antoine Minet; Steven Melvin; Marc Metian; Angus Taylor; François Oberhänsli; Christel Lefrançois; Peter Swarzenski; Paco Bustamante; Thomas Lacoue-Labarthe

doi:10.1016/j.marenvres.2025.107013

Metabolomic and phenotypic effects of ocean acidification on cuttlefish differ across early life stages

Antoine Minet, Steven Melvin, Marc Metian, Angus Taylor, François Oberhänsli, Christel Lefrançois, Peter Swarzenski, Paco Bustamante, Thomas Lacoue-Labarthe

Biodiversity and Ecosystem Health

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Ocean acidification (OA) affects the physiology and behaviour of some marine organisms, impacting their development and metabolism during vulnerable early-life stages. Among them, the embryo of the cuttlefish develops for about two months in encapsulated eggs with harsh perivitelline conditions of hypoxia and hypercapnia, potentially worsened by OA. In this study, common cuttlefish Sepia officinalis embryos and juveniles, were exposed to five pH conditions (pH_T 8.08 to 7.43). Growth, development and metabolite profiles were explored during the embryonic development period up to 10 days-post-hatching. Our results show delayed embryonic development and decreased hatching success at pH 7.43, but no effect on juvenile weight upon hatching. The ¹H Nuclear Magnetic Resonance (NMR) spectroscopy revealed that decreasing pH affected metabolites profiles in embryos until a metabolic suppression was observed at pH 7.43. The O₂ consumption in 10d-old juveniles did not change with pH whereas metabolites indicated a switch to anaerobic metabolism under low pH. Overall, our results suggest that the transition from the encapsulated embryonic stage to the free juvenile life shapes a metabolomic reprogramming more drastically than ocean acidification.

Original language	English
Article number	107013
Journal	Marine Environmental Research
Volume	205
DOIs	https://doi.org/10.1016/j.marenvres.2025.107013
State	Published - Mar 2025

Funding

This work is a contribution to the MERCy project funded by la Fondation pour la Recherche sur la Biodiversit\u00E9 and the Minist\u00E8re de la Transition Ecologique et Solidaire. The R\u00E9gion Nouvelle Aquitaine is acknowledged for its support to the PhD grant to AM through the EXPO project. Authors warmly thank Pierre Rideau and the \u201CPort de Plaisance de La Rochelle\u201D for providing with the cuttlefish eggs. The Institut Universitaire de France (IUF) is acknowledged for its support to PB as a Senior Member. MM, AT, FO, and PWS are grateful for the support provided to the Environment Laboratories by the government of the Principality of Monaco.

Keywords

Cephalopods
Growth
Metabolite
NMR
Respirometry
Sepia officinalis
pCO/ pH

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10.1016/j.marenvres.2025.107013

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title = "Metabolomic and phenotypic effects of ocean acidification on cuttlefish differ across early life stages",

abstract = "Ocean acidification (OA) affects the physiology and behaviour of some marine organisms, impacting their development and metabolism during vulnerable early-life stages. Among them, the embryo of the cuttlefish develops for about two months in encapsulated eggs with harsh perivitelline conditions of hypoxia and hypercapnia, potentially worsened by OA. In this study, common cuttlefish Sepia officinalis embryos and juveniles, were exposed to five pH conditions (pHT 8.08 to 7.43). Growth, development and metabolite profiles were explored during the embryonic development period up to 10 days-post-hatching. Our results show delayed embryonic development and decreased hatching success at pH 7.43, but no effect on juvenile weight upon hatching. The 1H Nuclear Magnetic Resonance (NMR) spectroscopy revealed that decreasing pH affected metabolites profiles in embryos until a metabolic suppression was observed at pH 7.43. The O2 consumption in 10d-old juveniles did not change with pH whereas metabolites indicated a switch to anaerobic metabolism under low pH. Overall, our results suggest that the transition from the encapsulated embryonic stage to the free juvenile life shapes a metabolomic reprogramming more drastically than ocean acidification.",

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author = "Antoine Minet and Steven Melvin and Marc Metian and Angus Taylor and Fran{\c c}ois Oberh{\"a}nsli and Christel Lefran{\c c}ois and Peter Swarzenski and Paco Bustamante and Thomas Lacoue-Labarthe",

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AU - Oberhänsli, François

AU - Lefrançois, Christel

AU - Swarzenski, Peter

AU - Bustamante, Paco

AU - Lacoue-Labarthe, Thomas

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N2 - Ocean acidification (OA) affects the physiology and behaviour of some marine organisms, impacting their development and metabolism during vulnerable early-life stages. Among them, the embryo of the cuttlefish develops for about two months in encapsulated eggs with harsh perivitelline conditions of hypoxia and hypercapnia, potentially worsened by OA. In this study, common cuttlefish Sepia officinalis embryos and juveniles, were exposed to five pH conditions (pHT 8.08 to 7.43). Growth, development and metabolite profiles were explored during the embryonic development period up to 10 days-post-hatching. Our results show delayed embryonic development and decreased hatching success at pH 7.43, but no effect on juvenile weight upon hatching. The 1H Nuclear Magnetic Resonance (NMR) spectroscopy revealed that decreasing pH affected metabolites profiles in embryos until a metabolic suppression was observed at pH 7.43. The O2 consumption in 10d-old juveniles did not change with pH whereas metabolites indicated a switch to anaerobic metabolism under low pH. Overall, our results suggest that the transition from the encapsulated embryonic stage to the free juvenile life shapes a metabolomic reprogramming more drastically than ocean acidification.

AB - Ocean acidification (OA) affects the physiology and behaviour of some marine organisms, impacting their development and metabolism during vulnerable early-life stages. Among them, the embryo of the cuttlefish develops for about two months in encapsulated eggs with harsh perivitelline conditions of hypoxia and hypercapnia, potentially worsened by OA. In this study, common cuttlefish Sepia officinalis embryos and juveniles, were exposed to five pH conditions (pHT 8.08 to 7.43). Growth, development and metabolite profiles were explored during the embryonic development period up to 10 days-post-hatching. Our results show delayed embryonic development and decreased hatching success at pH 7.43, but no effect on juvenile weight upon hatching. The 1H Nuclear Magnetic Resonance (NMR) spectroscopy revealed that decreasing pH affected metabolites profiles in embryos until a metabolic suppression was observed at pH 7.43. The O2 consumption in 10d-old juveniles did not change with pH whereas metabolites indicated a switch to anaerobic metabolism under low pH. Overall, our results suggest that the transition from the encapsulated embryonic stage to the free juvenile life shapes a metabolomic reprogramming more drastically than ocean acidification.

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Metabolomic and phenotypic effects of ocean acidification on cuttlefish differ across early life stages

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