Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis

Sebastian Baumgarten, Maha Joana Cziesielski, Ludivine Thomas, Craig Michell, Lisl Y. Esherick, John R. Pringle, Manuel Aranda, Christian R. Voolstra

Research output: Contribution to journalArticlepeer-review

33 Scopus citations

Abstract

Reef-building corals and other cnidarians living in symbiotic relationships with intracellular, photosynthetic dinoflagellates in the genus Symbiodinium undergo transcriptomic changes during infection with the algae and maintenance of the endosymbiont population. However, the precise regulatory mechanisms modulating the host transcriptome are unknown. Here we report apparent post-transcriptional gene regulation by miRNAs in the sea anemone Aiptasia, a model system for cnidarian-dinoflagellate endosymbiosis. Aiptasia encodes mainly species-specific miRNAs, and there appears to have been recent differentiation within the Aiptasia genome of miRNAs that are commonly conserved among anthozoan cnidarians. Analysis of miRNA expression showed that both conserved and species-specific miRNAs are differentially expressed in response to endosymbiont infection. Using cross-linking immunoprecipitation of Argonaute, the central protein of the miRNA-induced silencing complex, we identified miRNA binding sites on a transcriptome-wide scale and found that the targets of the miRNAs regulated in response to symbiosis include genes previously implicated in biological processes related to Symbiodinium infection. Our study shows that cnidarian miRNAs recognize their mRNA targets via high-complementarity target binding and suggests that miRNA-mediated modulations of genes and pathways are important during the onset and maintenance of cnidarian-dinoflagellate endosymbiosis. This article is protected by copyright. All rights reserved.
Original languageEnglish (US)
Pages (from-to)403-418
Number of pages16
JournalMolecular Ecology
Volume27
Issue number2
DOIs
StatePublished - Dec 23 2017

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: Research reported in this publication was supported by the King Abdullah University of Science and Technology (KAUST) and by Gordon and Betty Moore Foundation Grant 2629.01 (to J.R.P.). We thank the Bioscience Core lab and the Imaging and Characterization Core lab at KAUST for help with the protein characterization and microscopy. Figure 5 was created by Heno Hwang, scientific illustrator at KAUST.

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