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Adaptive metabolic reprogramming conserves energy status in Antarctic giants


Abstract

Polar marine invertebrate giants are proposed to have emerged from the greater availability of environmental oxygen, overcoming the viscosity of cold water and avoiding oxygen poisoning. However, molecular evidence on their metabolic adaptations is lacking to date. Consequently, we characterised the metabolome profiles of a number of marine Antarctic giants and their regular-size relatives exposed acutely in the laboratory either under mean seasonal conditions or elevated temperature. Giants from very distinct taxa share the differential utilisation of metabolic pathways involved in energy production, suggesting an adaptive convergence of metabolic reprogramming to meet the challenge of possessing larger bodies and facing harsh polar conditions. Further, we show that giants are not just larger regular-size species, as indicated by a breakpoint in the allometric relationship for metabolomics scores. Finally, giants do not appear to be more sensitive to ocean warming when compared to their regular-size relatives, all species tested showing no short-term metabolomics reprogramming under elevated temperatures.

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Acknowledgements

We wish to thank the Instituto Antártico Chileno (INACH) (Punta Arenas, Chile) and the staff of the INACH Antarctic Research Station Profesor Julio Escudero on King-George Island in Antarctica for enabling our research stay, and for their support with scientific diving, field collections, and storage and transport of frozen specimens to the Centro de Investigación Dinámica de Ecosistemas Marinos de Altas Latitudes (CENTRO IDÉAL) in Punta Arenas (Chile). In particular, we wish to thank Rodrigo Molina, Juan Bravo, Daniel Ramirez, Constanza Mendoza for their technical and logistical support. We are also grateful to Catalina Silva for her help with processing rapidly the specimens at the end of the experiment, and the entire Pardo Lab for their help under and above water, with particular mention to Sebastian Gonzalez, Javiera Sanhueza and Hans Jaramillo. PC is extremely grateful to the extremely professional team of the Chilean Navy operating the Galvarino cargo ship, for granting him safe and fast passage through the unforgiving and unforgettable waters of the Drake Passage and Beagle Canal back to Punta Arenas. Thanks also go to the CENTRO IDÉAL (and in particular Angelica Saldivia and Hermes Andrade) for the logistic organization and for their help with the storage and transport of frozen specimens to UQAR in Rimouski (QC, Canada). Antarctic invertebrate specimens were collected and transported to the MEEP Laboratory in Rimouski (QC, Canada) under the Instituto Antártico Chileno (INACH) certificate No. 284/2023. All experimental procedures and sample handling complied with the ethical guidelines for the use of animals in research established by the National Commission for Scientific and Technological Research (CONICYT, Chile), FONDAP-IDEAL 15150003, and the Universidad Austral de Chile, and were conformed to the ARRIVE guidelines.

Funding

This work was supported by: (i) a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant (RGPIN-2020–05627) and (ii) a Canada Foundation for Innovation grant both to PC, and (iii) a Centro IDÉAL Project No. 15150003 funded by the Agencia Nacional de investigación y desarrollo (ANID). LF acknowledges support from MITACS Accelerate (IT35557) and FRQNT PBEEE (350373).

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Piero Calosi.

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Supplementary Information

41598_2026_56044_MOESM1_ESM.zip (download ZIP )

Supplementary Information 1. ESM1: Animated GIF file showing the Principal Component Analysis (PCA) of the metabolome profile across all 108 samples, for each term of interest, i.e., per treatment (top row), taxonomic group (middle row) and gigantism status (bottom row). Axes show the first (PC1), second (PC3) and third (PC3) principal components. Groups are shown in blue (‘cold’ treatment) and red (‘hot’ treatment) in the top row; in pale beige (Amphipoda), dark grey (Pycnogonida) and magenta (Ophiuroidea) in the middle row; and in green (regular-size species) and orange (giant species) in the bottom row. Built using the scatter3d function from the car R package with default parameters, i.e., ellipsoids showing an expected proportion of bivariate-normal distribution of 0.5. Points are individual specimens’ samples. ESM2: Animated GIF file showing the Principal Component Analysis (PCA) of the metabolome profile of giant versus regular-size species per taxonomic group: Amphipoda (top row), Pycnogonida (middle row) and Ophiuroidea (bottom row). Axes show the first (PC1), second (PC3) and third (PC3) principal components. Groups are shown in green (regular-size species) and orange (giant species). Built using the scatter3d function from the car R package with default parameters, i.e., ellipsoids showing an expected proportion of bivariate-normal distribution of 0.5. Points are individual specimens’ samples. ESM3: Interactive version of the networks shown in Figure 4G, H and I. Data shows the FELLA metabolome networks per taxonomic group: Amphipoda (A), Pycnogonida (B) and Ophiuroidea (C). Differentially Abundant Metabolites (SDM) are shown as ‘input compound’ (star icons) that were used to generate the networks in FELLA. SDM are highlighted with their log2-fold change direction calculated from limma with upward and downward arrows indicating an increase and decrease, respectively, in giants relative to regular-size species. Network statistics computed by FELLA and Cytoscape are shown as interactive labels when hovering on nodes and edges. By default, KEGG pathways and input compounds are highlighted by the user can show different nodes by selecting on the ‘Select by id’ option. Built using the FELLA and visNetwork R packages. Access ESM3 online here file:///Users/pierocalosi/Downloads/ESM3_Network.per.taxon.html. Dataset SD1: dataset containing multiple data tables about the metabolomics data. The dataset contains all raw and processed metabolomic data, the limma analyses, and the functional analyses using MetaboAnalyst and FELLA. Information about the metabolites is also provided. All details about each individual data tables are given in the ‘Read.me (content)’ and ‘Read.me (metadata)’ tabs.

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Calosi, P., Feugere, L., Vermandele, F. et al. Adaptive metabolic reprogramming conserves energy status in Antarctic giants.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-56044-0

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