Frontloading of stress response genes enhances robustness to environmental change in chimeric corals

Jeremie Vidal-Dupiol, Erwan Harscouet, Dor Shefy, Eve Toulza, Olivier Rey, Jean François Allienne, Guillaume Mitta, Baruch Rinkevich

Research output: Contribution to journalArticlepeer-review

Abstract

Background: Chimeras are genetically mixed entities resulting from the fusion of two or more conspecifics. This phenomenon is widely distributed in nature and documented in a variety of animal and plant phyla. In corals, chimerism initiates at early ontogenic states (larvae to young spat) and results from the fusion between two or more closely settled conspecifics. When compared to genetically homogenous colonies (non-chimeras), the literature has listed ecological and evolutionary benefits for traits at the chimeric state, further positioning coral chimerism as an evolutionary rescue instrument. However, the molecular mechanisms underlying this suggestion remain unknown. Results: To address this question, we developed field monitoring and multi-omics approaches to compare the responses of chimeric and non-chimeric colonies acclimated for 1 year at 10-m depth or exposed to a stressful environmental change (translocation from 10- to 2-m depth for 48h). We showed that chimerism in the stony coral Stylophora pistillata is associated with higher survival over a 1-year period. Transcriptomic analyses showed that chimeras lose transcriptomic plasticity and constitutively express at higher level (frontload) genes responsive to stress. This frontloading may prepare the colony to face at any time environmental stresses which explain its higher robustness. Conclusions: These results show that chimeras are environmentally robust entities with an enhanced ability to cope with environmental stress. Results further document the potential usefulness of chimeras as a novel reef restoration tool to enhance coral adaptability to environmental change, and confirm that coral chimerism can be an evolutionary rescue instrument.

Original languageEnglish
Article number167
JournalBMC Biology
Volume20
Issue number1
DOIs
StatePublished - Dec 2022
Externally publishedYes

Bibliographical note

Funding Information:
We thank the Bio-Environment platform (University of Perpignan), Dr. Cristian Chaparro and the IHPE’ bioinformatics service, the GenoToul bioinformatics platform, the Toulouse Midi-Pyrenees and Sigenae group for providing help and computing resources (Galaxy instance; http://sigenae-workbench.toulouse.inra.fr), the Ifremer Bioinformatics Core Facility (SeBiMER; https://ifremer-bioinformatics.github.io/) for providing technical help in bioinformatic, the Pôle de Calcul et de Données Marines (PCDM; https://wwz.ifremer.fr/en/Research-Technology/Research-Infrastructures/Digital-infrastructures/Computation-Centre) for providing DATARMOR computing and storage resources and to G. Paz for helping with the figures. This study is set within the framework of the “Laboratoire d’Excellence (LABEX)” TULIP (ANR-10-LABX-41).

Funding Information:
This project was funded by the Israeli-French high council for scientific & technological research program (Maïmonide-Israel), by the joint NSFC-ISF research program (nos. 42161144006 and 3511/21, respectively) and by Barrett Foundation.

Publisher Copyright:
© 2022, The Author(s).

Keywords

  • Chimera
  • Corals
  • Environmental change
  • Global change
  • Plasticity/robustness
  • Transcriptomics

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology (all)
  • Agricultural and Biological Sciences (all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

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