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

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.

Metrics

  • 1,632
    Page views
  • 297
    Downloads
  • 22
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Emilie-Fleur Neubaeur
  2. Angela Z Poole
  3. Philipp Neubauer
  4. Olivier Detournay
  5. Kenneth Tan
  6. Simon K Davy
  7. Virginia M Weis
(2017)
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

Further reading

    1. Ecology
    2. Evolutionary Biology
    Dakota E McCoy, Benjamin Goulet-Scott ... John Kartesz
    Tools and Resources

    Sustainable cities depend on urban forests. City trees-pillars of urban forests - improve our health, clean the air, store CO2, and cool local temperatures. Comparatively less is known about city tree communities as ecosystems, particularly regarding spatial composition, species diversity, tree health, and the abundance of introduced species. Here, we assembled and standardized a new dataset of N=5,660,237 trees from 63 of the largest US cities with detailed information on location, health, species, and whether a species is introduced or naturally occurring (i.e., 'native'). We further designed new tools to analyze spatial clustering and the abundance of introduced species. We show that trees significantly cluster by species in 98% of cities, potentially increasing pest vulnerability (even in species-diverse cities). Further, introduced species significantly homogenize tree communities across cities, while naturally occurring trees (i.e., 'native' trees) comprise 0.51%-87.3% (median=45.6%) of city tree populations. Introduced species are more common in drier cities, and climate also shapes tree species diversity across urban forests. Parks have greater tree species diversity than urban settings. Compared to past work which focused on canopy cover and species richness, we show the importance of analyzing spatial composition and introduced species in urban ecosystems (and we develop new tools and datasets to do so). Future work could analyze city trees and socio-demographic variables or bird, insect, and plant diversity (e.g., from citizen-science initiatives). With these tools, we may evaluate existing city trees in new, nuanced ways and design future plantings to maximize resistance to pests and climate change. We depend on city trees.

    1. Ecology
    2. Evolutionary Biology
    Nicholas Grebe, Jean Paul Hirwa ... Stacy Rosenbaum
    Research Article

    Evolutionary theories predict that sibling relationships will reflect a complex balance of cooperative and competitive dynamics. In most mammals, dispersal and death patterns mean that sibling relationships occur in a relatively narrow window during development, and/or only with same-sex individuals. Besides humans, one notable exception are mountain gorillas, in which non-sex biased dispersal, relatively stable group composition, and the long reproductive tenures of alpha males mean that animals routinely reside with both maternally and paternally related siblings, of the same and opposite sex, throughout their lives. Using nearly 40,000 hours of behavioral data collected over 14 years on 699 sibling and 1235 non-sibling pairs of wild mountain gorillas, we demonstrate that individuals have strong affiliative preferences for full and maternal siblings over paternal siblings or unrelated animals, consistent with an inability to discriminate paternal kin. Intriguingly, however, aggression data imply the opposite. Aggression rates were statistically indistinguishable among all types of dyads except one: in mixed-sex dyads, non-siblings engaged in substantially more aggression than siblings of any type. This pattern suggests mountain gorillas may be capable of distinguishing paternal kin, but nonetheless choose not to affiliate with them over non-kin. We observe a preference for maternal kin in a species with high reproductive skew (i.e., high relatedness certainty), even though low reproductive skew (i.e., low relatedness certainty) is believed to underlie such biases in other non-human primates. Our results call into question reasons for strong maternal kin biases when paternal kin are identifiable, familiar, and similarly likely to be long-term groupmates, and they may also suggest behavioral mismatches at play during a transitional period in mountain gorilla society.