The Genome of Aiptasia, a Sea Anemone Model for Coral Symbiosis
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The genome of Aiptasia, a sea anemone model for coral symbiosis Sebastian Baumgartena, Oleg Simakovb,1, Lisl Y. Esherickc, Yi Jin Liewa, Erik M. Lehnertc, Craig T. Michella, Yong Lia, Elizabeth A. Hambletonb, Annika Guseb, Matt E. Oatesd, Julian Goughd, Virginia M. Weise, Manuel Arandaa, John R. Pringlec,2, and Christian R. Voolstraa,2 aRed Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia; bCentre for Organismal Studies, Heidelberg University, 69120 Heidelberg, Germany; cDepartment of Genetics, Stanford University School of Medicine, Stanford, CA 94305; dDepartment of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom; and eDepartment of Integrative Biology, Oregon State University, Corvallis, OR 97331 Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved August 4, 2015 (received for review July 8, 2015) The most diverse marine ecosystems, coral reefs, depend upon a a solid platform for research on Aiptasia, we have sequenced and functional symbiosis between a cnidarian animal host (the coral) and analyzed its genome. The results have already provided important intracellular photosynthetic dinoflagellate algae. The molecular and insights into several aspects of the evolution and function of the cellular mechanisms underlying this endosymbiosis are not well symbiotic system. understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable lab- Results and Discussion oratory model for investigating these mechanisms. Here we report on Genome Size and Assembly. We used flow cytometry to estimate the the assembly and analysis of the Aiptasia genome, which will provide haploid genome size of Aiptasia, obtaining a value of ∼260 Mb (SI a foundation for future studies and has revealed several features that Appendix, Fig. S2 A, 1–3). This value is smaller than those reported may be key to understanding the evolution and function of the en- previously for three other cnidarians (SI Appendix,TableS1), in- dosymbiosis. These features include genomic rearrangements and tax- cluding two other anthozoans, the anemone Nematostella vectensis onomically restricted genes that may be functionally related to the (450 Mb) (8) and the stony coral Acropora digitifera (420 Mb) (9). symbiosis, aspects of host dependence on alga-derived nutrients, However, we estimated a genome size of ∼329 Mb for N. vectensis a novel and expanded cnidarian-specific family of putative pattern- by flow cytometry (SI Appendix,Fig.S2A, 4–6), and a previous recognition receptors that might be involved in the animal–algal in- independent estimate by densitometry of Feulgen-stained embry- teractions, and extensive lineage-specific horizontal gene transfer. Ex- onic nuclei gave an even lower value of ∼220 Mb (10). tensive integration of genes of prokaryotic origin, including genes for To generate a genome sequence, we used DNA from a clonal antimicrobial peptides, presumably reflects an intimate association of population of aposymbiotic anemones to obtain ∼140× coverage the animal–algal pair also with its prokaryotic microbiome. by Illumina short-read sequencing plus additional sequence from long-insert mate-pair libraries (SI Appendix, Table S2). From these coral reefs | endosymbiosis | horizontal gene transfer | dinoflagellate | sequences we assembled a draft genome of ∼258 Mb comprised of pattern-recognition receptors 5,065 scaffolds and 29,410 contigs, with half of the genome found in scaffolds longer than 440 kb and in contigs longer than 14.9 kb oral reefs form marine-biodiversity hotspots that are of enor- Cmous ecological, economic, and aesthetic importance. Coral Significance growth and reef deposition are based energetically on the endo- symbiosis between the cnidarian animal hosts and photosynthetic Coral reefs form marine-biodiversity hotspots of enormous eco- SCIENCES dinoflagellate algae of the genus Symbiodinium, which live in vesicles logical, economic, and aesthetic importance that rely energetically ENVIRONMENTAL within the gastrodermal (gut) cells of the animal and typically supply on a functional symbiosis between the coral animal and a pho- ≥90% of its total energy, while the host provides the algae with a tosynthetic alga. The ongoing decline of corals worldwide due to sheltered environment and the inorganic nutrients needed for pho- anthropogenic influences, including global warming, ocean acidi- tosynthesis and growth (1). This tight metabolic coupling allows the fication, and pollution, heightens the need for an experimentally holobiont (i.e., the animal host and its microbial symbionts) to thrive tractable model system to elucidate the molecular and cellular in nutrient-poor waters. Although the ecology of coral reefs has been biology underlying the symbiosis and its susceptibility or resilience studied intensively, the molecular and cellular mechanisms un- to stress. The small sea anemone Aiptasia is such a system, and derlying the critical endosymbiosis remain poorly understood (2). As our analysis of its genome provides a foundation for research in coral reefs face an ongoing and increasing threat from anthropogenic this area and has revealed numerous features of interest in re- environmental change (3), new insights into these mechanisms are of lation to the evolution and function of the symbiotic relationship. critical importance to understanding the resilience and adaptability of coral reefs and thus to the planning of conservation strategies (4). 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. Aiptasia is a globally distributed sea anemone that harbors en- 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. ana- dosymbiotic Symbiodinium like its Class Anthozoa relatives the lyzed data; and S.B., O.S., L.Y.E., Y.J.L., J.R.P., and C.R.V. wrote the paper. stony corals (Fig. 1 and SI Appendix,Fig.S1A) (4, 5). Aiptasia The authors declare no conflict of interest. has a range of polyp sizes convenient for experimentation and This article is a PNAS Direct Submission. is easily grown in laboratory culture, where it reproduces both Freely available online through the PNAS open access option. asexually (so that large clonal populations can be obtained) and Data deposition: The data reported in this paper are available at aiptasia.reefgenomics. sexually (allowing experiments on larvae and potentially genetic org and have been deposited in the NCBI database (accession no. PRJNA261862). studies), and it can be maintained indefinitely in an aposymbiotic 1Present address: Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan. (dinoflagellate-free) state and reinfected by a variety of Symbiodi- 2To whom correspondence may be addressed. Email: [email protected] or nium strains (6, 7). These characteristics make Aiptasia ahighlyat- [email protected]. tractive model system for studies of the molecular and cellular This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. basis of the cnidarian–dinoflagellate endosymbiosis (2, 4). To provide 1073/pnas.1513318112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1513318112 PNAS | September 22, 2015 | vol. 112 | no. 38 | 11893–11898 Downloaded by guest on October 1, 2021 A This is similar to previously reported findings with other animals (11). About half of these synteny blocks, containing 1,727 genes, are shared only with one or more other cnidarians. Interestingly, al- though many of the Aiptasia HOX genes are in clusters, as in other metazoans, the detailed organization of the clusters is distinct even from that in other anthozoans, leaving the ancestral organization of the HOX cluster uncertain (15, 16) (Fig. 2B and Dataset S1.2). BCD To seek further insights into Aiptasia evolution and symbiosis, we identified the gene families with elevated rates of amino acid sub- stitution relative to other cnidarians (SI Appendix, SI Materials and Methods). Among 2,478 gene families, 143 (containing 165 genes) were found to show accelerated evolution (Dataset S1.3), but anal- Fig. 1. Phylogenetic position and different symbiotic states of Aiptasia. ysis of the functions ascribed to these families did not reveal obvious (A) Partial phylogenetic tree (see SI Appendix, SI Materials and Methods clues to the molecular basis of the endosymbiotic relationship. and Fig. S1A for details) shows Aiptasia grouped with other anthozoans among the cnidarians. Numbers on nodes denote bootstrap values. Taxonomically Restricted Genes. We found 3,107 genes whose pre- (B–D) An aposymbiotic Aiptasia polyp (B) and symbiotic polyps viewed under white light (C) or by fluorescence microscopy to visualize the dicted products had no discernible homologs in other organisms red chlorophyll autofluorescence of the endosymbiotic Symbiodinium (SI Appendix, Table S6). Of these, 1,946 were supported by tran- algae (D). scriptomic evidence. Such taxonomically restricted genes (TRGs) are thought to play important roles in the creation of evolutionary (Table 1 and SI Appendix, Table S3). Using ab initio prediction novelties and morphological diversity within the taxonomic group informed by a reference transcriptome covering several de- (17, 18). Although the TRG products