A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian-dinoflagellate symbiosis
- Victoria University of Wellington, New Zealand
- Western Oregon University, United States
- Dragonfly Data Science, New Zealand
- Planktovie sas, France
- Oregon State University, United States
Abstract
The mutualistic endosymbiosis between cnidarians and dinoflagellates is mediated by complex inter-partner signaling events, where the host cnidarian innate immune system plays a crucial role in recognition and regulation of symbionts. To date, little is known about the diversity of thrombospondin-type-1 repeat (TSR) domain proteins in basal metazoans and or their potential role in regulation of cnidarian-dinoflagellate mutualisms. We reveal a large and diverse repertoire of TSR proteins in seven anthozoan species, and show that in the model sea anemone Aiptasia pallida the TSR domain promotes colonization of the host by the symbiotic dinoflagellate Symbiodinium minutum. Blocking TSR domains led to decreased colonization success, while adding exogenous TSRs resulted in a 'super colonization'. Furthermore, gene expression of TSR proteins was highest at early time-points during symbiosis establishment. Our work characterizes the diversity of cnidarian TSR proteins and provides evidence that these proteins play an important role in the establishment of cnidarian-dinoflagellate symbiosis.
Data availability
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Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organizationPublicly available at NCBI BioProject (accession no. PRJNA19965). This work used the following resource built from this data: http://genome.jgi.doe.gov/Nemve1/Nemve1.home.html.
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Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organizationPublicly available at NCBI BioProject (accession no. PRJNA12581). This work used the following resource built from this data: http://genome.jgi.doe.gov/Nemve1/Nemve1.home.html.
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Data from: De novo assembly and characterization of four anthozoan (phylum Cnidaria) transcriptomesAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication. This work used the following resource built from this data: http://people.oregonstate.edu/~meyere/data.htm.
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Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: the transcriptome of aposymbiotic A. pallidaPublicly available at the NCBI Sequence Read Archive (accession no. SRR696721). This work used the following resource built from this data: http://pringlelab.stanford.edu/projects.html.
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The genome of Aiptasia, a sea anemone model for coral symbiosisPublicly available at NCBI BioProject (accession no. PRJNA261862). This work uses the following resource built from this data: http://aiptasia.reefgenomics.org/.
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Using the Acropora digitifera genome to understand coral responses to environmental changePublicly available at NCBI BioProject (accession no. PRJNA314803). This work uses the following resource built from this data: http://marinegenomics.oist.jp/coral/viewer/info?project_id=3.
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Using the Acropora digitifera genome to understand coral responses to environmental changePublicly available at NCBI BioProject (accession no. PRJDA67425). This work uses the following resource built from this data: http://marinegenomics.oist.jp/coral/viewer/info?project_id=3.
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Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcificationPublicly available at NCBI BioProject (accession no. PRJNA74409). This work uses the following resource built from this data: http://www.bio.utexas.edu/research/matz_lab/matzlab/Data.html.
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Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structurePublicly available at NCBI BioProject (accession no. PRJDB732). This work uses the following resource built from this data: http://marinegenomics.oist.jp/symb/viewer/info?project_id=21.
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Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestylePublicly available at NCBI BioProject (accession no. PRJNA292355). This work uses the following resource built from this data: http://smic.reefgenomics.org/.
Article and author information
Author details
Funding
National Science Foundation (IOB0919073)
- Virginia M Weis
Victoria University of Wellington
- Emilie-Fleur Neubauer
Oregon State University
- Kenneth Tan
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2017, Neubauer et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian-dinoflagellate symbiosis
eLife 6:e24494.
https://doi.org/10.7554/eLife.24494
