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Research Article

The genome of Aiptasia, a sea anemone model for coral symbiosis

Sebastian Baumgarten, Oleg Simakov, Lisl Y. Esherick, Yi Jin Liew, Erik M. Lehnert, Craig T. Michell, View ORCID ProfileYong Li, Elizabeth A. Hambleton, Annika Guse, Matt E. Oates, Julian Gough, Virginia M. Weis, View ORCID ProfileManuel Aranda, John R. Pringle, and Christian R. Voolstra
  1. aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
  2. bCentre for Organismal Studies, Heidelberg University, 69120 Heidelberg, Germany;
  3. cDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305;
  4. dDepartment of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom;
  5. eDepartment of Integrative Biology, Oregon State University, Corvallis, OR 97331

See allHide authors and affiliations

PNAS September 22, 2015 112 (38) 11893-11898; first published August 31, 2015; https://doi.org/10.1073/pnas.1513318112
Sebastian Baumgarten
aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
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Oleg Simakov
bCentre for Organismal Studies, Heidelberg University, 69120 Heidelberg, Germany;
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Lisl Y. Esherick
cDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305;
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Yi Jin Liew
aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
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Erik M. Lehnert
cDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305;
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Craig T. Michell
aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
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Yong Li
aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
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  • ORCID record for Yong Li
Elizabeth A. Hambleton
bCentre for Organismal Studies, Heidelberg University, 69120 Heidelberg, Germany;
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Annika Guse
bCentre for Organismal Studies, Heidelberg University, 69120 Heidelberg, Germany;
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Matt E. Oates
dDepartment of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom;
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Julian Gough
dDepartment of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom;
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Virginia M. Weis
eDepartment of Integrative Biology, Oregon State University, Corvallis, OR 97331
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Manuel Aranda
aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
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  • ORCID record for Manuel Aranda
John R. Pringle
cDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305;
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  • For correspondence: christian.voolstra@kaust.edu.sa jpringle@stanford.edu
Christian R. Voolstra
aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia;
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  • For correspondence: christian.voolstra@kaust.edu.sa jpringle@stanford.edu
  1. Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved August 4, 2015 (received for review July 8, 2015)

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Significance

Coral reefs form marine-biodiversity hotspots of enormous ecological, economic, and aesthetic importance that rely energetically on a functional symbiosis between the coral animal and a photosynthetic alga. The ongoing decline of corals worldwide due to anthropogenic influences, including global warming, ocean acidification, and pollution, heightens the need for an experimentally tractable model system to elucidate the molecular and cellular biology underlying the symbiosis and its susceptibility or resilience to stress. The small sea anemone Aiptasia is such a system, and our analysis of its genome provides a foundation for research in this area and has revealed numerous features of interest in relation to the evolution and function of the symbiotic relationship.

Abstract

The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between a cnidarian animal host (the coral) and intracellular photosynthetic dinoflagellate algae. The molecular and cellular mechanisms underlying this endosymbiosis are not well understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable laboratory model for investigating these mechanisms. Here we report on the assembly and analysis of the Aiptasia genome, which will provide a foundation for future studies and has revealed several features that may be key to understanding the evolution and function of the endosymbiosis. These features include genomic rearrangements and taxonomically restricted genes that may be functionally related to the symbiosis, aspects of host dependence on alga-derived nutrients, a novel and expanded cnidarian-specific family of putative pattern-recognition receptors that might be involved in the animal–algal interactions, and extensive lineage-specific horizontal gene transfer. Extensive integration of genes of prokaryotic origin, including genes for antimicrobial peptides, presumably reflects an intimate association of the animal–algal pair also with its prokaryotic microbiome.

  • coral reefs
  • endosymbiosis
  • horizontal gene transfer
  • dinoflagellate
  • pattern-recognition receptors

Footnotes

  • ↵1Present address: Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan.

  • ↵2To whom correspondence may be addressed. Email: christian.voolstra{at}kaust.edu.sa or jpringle{at}stanford.edu.
  • Author contributions: S.B., E.M.L., J.R.P., and C.R.V. designed research; S.B., O.S., Y.J.L., E.M.L., C.T.M., Y.L., E.A.H., A.G., and M.A. performed research; M.E.O., J.G., V.M.W., and C.R.V. contributed new reagents/analytic tools; S.B., O.S., L.Y.E., Y.J.L., E.M.L., J.R.P., and C.R.V. analyzed data; and S.B., O.S., L.Y.E., Y.J.L., J.R.P., and C.R.V. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper are available at aiptasia.reefgenomics.org and have been deposited in the NCBI database (accession no. PRJNA261862).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1513318112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Symbiotic sea anemone genome
Sebastian Baumgarten, Oleg Simakov, Lisl Y. Esherick, Yi Jin Liew, Erik M. Lehnert, Craig T. Michell, Yong Li, Elizabeth A. Hambleton, Annika Guse, Matt E. Oates, Julian Gough, Virginia M. Weis, Manuel Aranda, John R. Pringle, Christian R. Voolstra
Proceedings of the National Academy of Sciences Sep 2015, 112 (38) 11893-11898; DOI: 10.1073/pnas.1513318112

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Symbiotic sea anemone genome
Sebastian Baumgarten, Oleg Simakov, Lisl Y. Esherick, Yi Jin Liew, Erik M. Lehnert, Craig T. Michell, Yong Li, Elizabeth A. Hambleton, Annika Guse, Matt E. Oates, Julian Gough, Virginia M. Weis, Manuel Aranda, John R. Pringle, Christian R. Voolstra
Proceedings of the National Academy of Sciences Sep 2015, 112 (38) 11893-11898; DOI: 10.1073/pnas.1513318112
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