1. Ecology
  2. Microbiology and Infectious Disease
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A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian-dinoflagellate symbiosis

  1. Emilie-Fleur Neubaeur
  2. Angela Z Poole
  3. Philipp Neubauer
  4. Olivier Detournay
  5. Kenneth Tan
  6. Simon K Davy  Is a corresponding author
  7. Virginia M Weis  Is a corresponding author
  1. Victoria University of Wellington, New Zealand
  2. Western Oregon University, United States
  3. Dragonfly Data Science, New Zealand
  4. Planktovie sas, France
  5. Oregon State University, United States
Research Article
  • Cited 17
  • Views 1,488
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Cite this article as: eLife 2017;6:e24494 doi: 10.7554/eLife.24494

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

The following previously published data sets were used
    1. Kitchen SA
    2. Crowder CM
    3. Poole AZ
    4. Weis VM
    5. Meyer E
    (2015) Data from: De novo assembly and characterization of four anthozoan (phylum Cnidaria) transcriptomes
    Available 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.
    1. Lehnert EM
    2. Burriesci MS
    3. Pringle JR
    (2012) Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: the transcriptome of aposymbiotic A. pallida
    Publicly 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.
    1. Baumgarten S
    2. Simakov O
    3. Esherick LY
    4. Liew YJ
    5. Lehnert EM
    6. Michell CT
    7. Li Y
    8. Hambleton EA
    9. Guse A
    10. Oates ME
    11. Gough J
    12. Weis VM
    13. Aranda M
    14. Pringle JR
    15. Voolstra CR
    (2015) The genome of Aiptasia, a sea anemone model for coral symbiosis
    Publicly available at NCBI BioProject (accession no. PRJNA261862). This work uses the following resource built from this data: http://aiptasia.reefgenomics.org/.
    1. Shinzato C
    2. Shoguchi E
    3. Kawashima T
    4. Hamada M
    5. Hisata K
    6. Tanaka M
    7. Fujie M
    8. Fujiwara M
    9. Koyanagi R
    10. Ikuta T
    11. Fujiyama A
    12. Miller DJ
    13. Satoh N
    (2011) Using the Acropora digitifera genome to understand coral responses to environmental change
    Publicly 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.
    1. Shinzato C
    2. Shoguchi E
    3. Kawashima T
    4. Hamada M
    5. Hisata K
    6. Tanaka M
    7. Fujie M
    8. Fujiwara M
    9. Koyanagi R
    10. Ikuta T
    11. Fujiyama A
    12. Miller DJ
    13. Satoh N
    (2011) Using the Acropora digitifera genome to understand coral responses to environmental change
    Publicly 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.
    1. Moya A
    2. Huisman L
    3. Ball EE
    4. Hayward DC
    5. Grasso LC
    6. Chua CM
    7. Woo HN
    8. Gattuso J-P
    9. Forêt S
    10. Miller DJ
    (2012) Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification
    Publicly 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.

Article and author information

Author details

  1. Emilie-Fleur Neubaeur

    School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
  2. Angela Z Poole

    Department of Biology, Western Oregon University, Monmouth, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Philipp Neubauer

    Dragonfly Data Science, Wellington, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4150-848X
  4. Olivier Detournay

    Planktovie sas, Allauch, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Kenneth Tan

    Department of Integrative Biology, Oregon State University, Corvallis, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Simon K Davy

    School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand
    For correspondence
    Simon.Davy@vuw.ac.nz
    Competing interests
    The authors declare that no competing interests exist.
  7. Virginia M Weis

    Department of Integrative Biology, Oregon State University, Corvallis, United States
    For correspondence
    weisv@oregonstate.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1826-2848

Funding

National Science Foundation (IOB0919073)

  • Virginia M Weis

Victoria University of Wellington

  • Emilie-Fleur Neubaeur

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.

Reviewing Editor

  1. Paul G Falkowski, Rutgers University, United States

Publication history

  1. Received: December 21, 2016
  2. Accepted: April 29, 2017
  3. Accepted Manuscript published: May 8, 2017 (version 1)
  4. Accepted Manuscript updated: May 9, 2017 (version 2)
  5. Version of Record published: May 26, 2017 (version 3)

Copyright

© 2017, Neubaeur 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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