Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite

Sarah Séité; Mark C. Harrison; David Sillam-Dussès; Roland Lupoli; Tom J. M. Van Dooren; Alain Robert; Laure-Anne Poissonnier; Arnaud Lemainque; David Renault; Sébastien Acket; Muriel Andrieu; José Viscarra; Hei Sook Sul; Z. Wilhelm de Beer; Erich Bornberg-Bauer; Mireille Vasseur-Cognet

doi:10.1038/s42003-021-02974-6

Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite

Sarah Séité, Mark C. Harrison, David Sillam-Dussès, Roland Lupoli, Tom J. M. Van Dooren, Alain Robert, Laure-Anne Poissonnier, Arnaud Lemainque, David Renault, Sébastien Acket, Muriel Andrieu, José Viscarra, Hei Sook Sul, Z. Wilhelm de Beer, Erich Bornberg-Bauer, Mireille Vasseur-Cognet

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Abstract

Kings and queens of eusocial termites can live for decades, while queens sustain a nearly maximal fertility. To investigate the molecular mechanisms underlying their long lifespan, we carried out transcriptomics, lipidomics and metabolomics in Macrotermes natalensis on sterile short-lived workers, long-lived kings and five stages spanning twenty years of adult queen maturation. Reproductives share gene expression differences from workers in agreement with a reduction of several aging-related processes, involving upregulation of DNA damage repair and mitochondrial functions. Anti-oxidant gene expression is downregulated, while peroxidability of membranes in queens decreases. Against expectations, we observed an upregulated gene expression in fat bodies of reproductives of several components of the IIS pathway, including an insulin-like peptide, Ilp9. This pattern does not lead to deleterious fat storage in physogastric queens, while simple sugars dominate in their hemolymph and large amounts of resources are allocated towards oogenesis. Our findings support the notion that all processes causing aging need to be addressed simultaneously in order to prevent it.

Original language	English
Article number	44
Number of pages	16
Journal	Communications Biology
Volume	5
DOIs	https://doi.org/10.1038/s42003-021-02974-6
Publication status	Published - 13 Jan 2022
Externally published	Yes

Bibliographical note

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

Funder

This study was supported by the International Human Frontier Science Program RGP0060/2018 to M.V-C. S.S. was also supported by a fellowship from Université de Paris Est-Créteil (UPEC). A.L. acknowledges financial support from France Génomique (ANR-10-INBS-09-08).

Funding

This study was supported by the International Human Frontier Science Program RGP0060/2018 to M.V-C. S.S. was also supported by a fellowship from Université de Paris Est-Créteil (UPEC). A.L. acknowledges financial support from France Génomique (ANR-10-INBS-09-08).

Funders	Funder number
Human Frontier Science Program	RGP0060/2018
Université Paris Est Créteil Val de Marne
France Génomique	ANR-10-INBS-09-08

Keywords

Ageing
Metabolism

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10.1038/s42003-021-02974-6Licence: CC BY

Harrison2022VoRFinal published version, 3.8 MBLicence: CC BY

Cite this

Séité, S., Harrison, M. C., Sillam-Dussès, D., Lupoli, R., Dooren, T. J. M. V., Robert, A., Poissonnier, L.-A., Lemainque, A., Renault, D., Acket, S., Andrieu, M., Viscarra, J., Sul, H. S., Beer, Z. W. D., Bornberg-Bauer, E., & Vasseur-Cognet, M. (2022). Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite. Communications Biology, 5, Article 44. https://doi.org/10.1038/s42003-021-02974-6

Séité, S, Harrison, MC, Sillam-Dussès, D, Lupoli, R, Dooren, TJMV, Robert, A, Poissonnier, L-A, Lemainque, A, Renault, D, Acket, S, Andrieu, M, Viscarra, J, Sul, HS, Beer, ZWD, Bornberg-Bauer, E & Vasseur-Cognet, M 2022, 'Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite', Communications Biology, vol. 5, 44. https://doi.org/10.1038/s42003-021-02974-6

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Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite

Abstract

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