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

Handle URI:
http://hdl.handle.net/10754/626371
Title:
Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis
Authors:
Baumgarten, Sebastian ( 0000-0003-2646-7699 ) ; Cziesielski, Maha J.; Thomas, Ludivine; Michell, Craig; Esherick, Lisl Y.; Pringle, John R.; Aranda, Manuel ( 0000-0001-6673-016X ) ; Voolstra, Christian R. ( 0000-0003-4555-3795 )
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.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Red Sea Research Center (RSRC); Bioscience Core Lab
Citation:
Baumgarten S, Cziesielski MJ, Thomas L, Michell CT, Esherick LY, et al. (2017) Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis. Molecular Ecology. Available: http://dx.doi.org/10.1111/mec.14452.
Publisher:
Wiley-Blackwell
Journal:
Molecular Ecology
Issue Date:
8-Dec-2017
DOI:
10.1111/mec.14452
PubMed ID:
29218749
Type:
Article
ISSN:
0962-1083
Sponsors:
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.
Additional Links:
http://onlinelibrary.wiley.com/doi/10.1111/mec.14452/abstract
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Bioscience Core Lab; Biological and Environmental Sciences and Engineering (BESE) Division; Reef Genomics, part of the Global Ocean Genome Project

Full metadata record

DC FieldValue Language
dc.contributor.authorBaumgarten, Sebastianen
dc.contributor.authorCziesielski, Maha J.en
dc.contributor.authorThomas, Ludivineen
dc.contributor.authorMichell, Craigen
dc.contributor.authorEsherick, Lisl Y.en
dc.contributor.authorPringle, John R.en
dc.contributor.authorAranda, Manuelen
dc.contributor.authorVoolstra, Christian R.en
dc.date.accessioned2017-12-14T12:34:04Z-
dc.date.available2017-12-14T12:34:04Z-
dc.date.issued2017-12-08en
dc.identifier.citationBaumgarten S, Cziesielski MJ, Thomas L, Michell CT, Esherick LY, et al. (2017) Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis. Molecular Ecology. Available: http://dx.doi.org/10.1111/mec.14452.en
dc.identifier.issn0962-1083en
dc.identifier.pmid29218749-
dc.identifier.doi10.1111/mec.14452en
dc.identifier.urihttp://hdl.handle.net/10754/626371-
dc.description.abstractReef-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.en
dc.description.sponsorshipResearch 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.en
dc.publisherWiley-Blackwellen
dc.relation.urlhttp://onlinelibrary.wiley.com/doi/10.1111/mec.14452/abstracten
dc.rightsThis is the peer reviewed version of the following article: Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis, which has been published in final form at http://doi.org/10.1111/mec.14452. This article may be used for non-commercial purposes in accordance With Wiley Terms and Conditions for self-archiving.en
dc.subjectCoralen
dc.subjectAnemoneen
dc.subjectArgonauteen
dc.subjectAiptasiaen
dc.subjectCross-linking Immunoprecipitation (Clip)en
dc.titleEvidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosisen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.contributor.departmentBioscience Core Laben
dc.identifier.journalMolecular Ecologyen
dc.eprint.versionPost-printen
dc.contributor.institutionDepartment of Genetics; Stanford University School of Medicine; Stanford California USAen
kaust.authorBaumgarten, Sebastianen
kaust.authorCziesielski, Maha J.en
kaust.authorThomas, Ludivineen
kaust.authorMichell, Craigen
kaust.authorAranda, Manuelen
kaust.authorVoolstra, Christian R.en

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