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Peer-reviewedCC BY 4.0eLife

Light-entrained chromatin priming poises rapid metamorphosis in a marine sponge

  1. 1Centre for Marine Science and School of the Environment, The University of Queensland, Brisbane, Australia

Abstract

The most widespread animal life cycle includes a planktonic larval stage that is environmentally induced to settle and rapidly metamorphose into a benthic juvenile. Although this transition is critical for survival, how planetary cues such as light interact with local ecological signals to prepare the genome for such rapid reprogramming remains poorly understood. Here, using the sponge Amphimedon queenslandica, we integrate time-resolved transcriptomic and chromatin accessibility profiling across larval competence, settlement, and the first hours of metamorphosis. We show that diminishing light at sunset is associated with extensive chromatin remodelling in swimming larvae prior to settlement despite relatively modest changes in gene expression. Upon environmental induction by a coralline alga, metamorphosis is accompanied by the rapid and transient activation of a large suite of deeply conserved transcription factors (TFs), including AP-1/bZIP family members, whose binding motifs are enriched in newly accessible regulatory regions near differentially expressed genes. Larvae prevented from experiencing sunset by constant light fail to settle and instead adopt an alternative transcriptional and chromatin state characterised by widespread loss of accessibility and repression of competence-associated TFs, including the circadian regulator CLOCK and other bHLH-PAS factors. These observations support a model in which light-entrained transcriptional activity establishes an anticipatory, permissive chromatin landscape that enables immediate and coordinated transcriptional reprogramming upon environmental induction. We propose that such chromatin priming may represent a broadly deployed regulatory strategy underlying the speed and robustness of metamorphosis in biphasic animal life cycles.

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BibTeX
@article{yuan2026lightentrained,
  title = {{Light-entrained chromatin priming poises rapid metamorphosis in a marine sponge}},
  author = {Huifang Yuan and Oceane Blard and Zac Pujic and Bernard M Degnan and Sandie M Degnan},
  journal = {eLife},
  year = {2026},
  month = oct,
  doi = {10.7554/elife.111060},
  url = {https://elifesciences.org/articles/111060},
  note = {CC BY 4.0},
}
RIS
TY  - JOUR
TI  - Light-entrained chromatin priming poises rapid metamorphosis in a marine sponge
AU  - Huifang Yuan
AU  - Oceane Blard
AU  - Zac Pujic
AU  - Bernard M Degnan
AU  - Sandie M Degnan
PY  - 2026
DA  - 2026/10/27
JO  - eLife
DO  - 10.7554/elife.111060
UR  - https://elifesciences.org/articles/111060
AB  - The most widespread animal life cycle includes a planktonic larval stage that is environmentally induced to settle and rapidly metamorphose into a benthic juvenile. Although this transition is critical for survival, how planetary cues such as light interact with local ecological signals to prepare the genome for such rapid reprogramming remains poorly understood. Here, using the sponge Amphimedon queenslandica, we integrate time-resolved transcriptomic and chromatin accessibility profiling across larval competence, settlement, and the first hours of metamorphosis. We show that diminishing light at sunset is associated with extensive chromatin remodelling in swimming larvae prior to settlement despite relatively modest changes in gene expression. Upon environmental induction by a coralline alga, metamorphosis is accompanied by the rapid and transient activation of a large suite of deeply conserved transcription factors (TFs), including AP-1/bZIP family members, whose binding motifs are enriched in newly accessible regulatory regions near differentially expressed genes. Larvae prevented from experiencing sunset by constant light fail to settle and instead adopt an alternative transcriptional and chromatin state characterised by widespread loss of accessibility and repression of competence-associated TFs, including the circadian regulator CLOCK and other bHLH-PAS factors. These observations support a model in which light-entrained transcriptional activity establishes an anticipatory, permissive chromatin landscape that enables immediate and coordinated transcriptional reprogramming upon environmental induction. We propose that such chromatin priming may represent a broadly deployed regulatory strategy underlying the speed and robustness of metamorphosis in biphasic animal life cycles.
SN  - 2050-084X
ER  -