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. 2016 Dec 22:6:39734.
doi: 10.1038/srep39734.

Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

M Aranda  1 , Y Li  1 , Y J Liew  1 , S Baumgarten  1 , O Simakov  2 , M C Wilson  3 , J Piel  3 , H Ashoor  4 , S Bougouffa  4 , V B Bajic  4 , T Ryu  5 , T Ravasi  5 , T Bayer  1   6 , G Micklem  7 , H Kim  8 , J Bhak  8 , T C LaJeunesse  9 , C R Voolstra  1
Affiliations

Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle

M Aranda et al. Sci Rep. .

Abstract

Despite half a century of research, the biology of dinoflagellates remains enigmatic: they defy many functional and genetic traits attributed to typical eukaryotic cells. Genomic approaches to study dinoflagellates are often stymied due to their large, multi-gigabase genomes. Members of the genus Symbiodinium are photosynthetic endosymbionts of stony corals that provide the foundation of coral reef ecosystems. Their smaller genome sizes provide an opportunity to interrogate evolution and functionality of dinoflagellate genomes and endosymbiosis. We sequenced the genome of the ancestral Symbiodinium microadriaticum and compared it to the genomes of the more derived Symbiodinium minutum and Symbiodinium kawagutii and eukaryote model systems as well as transcriptomes from other dinoflagellates. Comparative analyses of genome and transcriptome protein sets show that all dinoflagellates, not only Symbiodinium, possess significantly more transmembrane transporters involved in the exchange of amino acids, lipids, and glycerol than other eukaryotes. Importantly, we find that only Symbiodinium harbor an extensive transporter repertoire associated with the provisioning of carbon and nitrogen. Analyses of these transporters show species-specific expansions, which provides a genomic basis to explain differential compatibilities to an array of hosts and environments, and highlights the putative importance of gene duplications as an evolutionary mechanism in dinoflagellates and Symbiodinium.

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Figures

Figure 1
Figure 1. Comparison of genomic composition of the genomes of Symbiodinium microadriaticum, Symbiodinium minutum, and Symbiodinium kawagutii.
Genes were classified by best hits against nr database into seven kingdom/subkingdom-level organismal groups: Archaea, Bacteria, Fungi, Metazoa, Plantae, Protista, and Viruses. Chord diagrams show (A) the fairly even number of matches from both Symbiodinium species to these seven groups respectively, and (B) the large overlap between Symbiodinium species when they were allowed to match against each other.
Figure 2
Figure 2
Pfam domain enrichment in protein sets of Symbiodinium microadriaticum, Symbiodinium minutum, and Symbiodinium kawagutii (A) in comparison to 16 reference eukaryotic genomes, (B) in comparison to other dinoflagellate transcriptomes, (C) among Symbiodinium genomes. Rows indicate distinct Pfam domains. Domain enrichment was estimated via Fisher’s exact test on domain ratios, colors represent z-scores, and samples were clustered by Euclidean distance. Species names providing reference genomes are abbreviated as per the following: Symbiodinium kawagutii (Skav), Symbiodinium minutum (Smin), Symbiodinium microadriaticum (Smic), Emiliania huxleyi (Ehux), Thalassiosira pseudonana (Tpseu), Chlamydomonas reinhardtii (Cre), Guillardia theta (Gthe), Capsaspora owczarzaki (Cow), Trypanosoma brucei gambiense (Tgb), Tetrahymena thermophila (Ttherm), Plasmodium falciparum (Pfl), Arabidopsis thaliana (Ath), Amphimedon queenslandica (Aqu), Stylophora pistillata (Spis), Trichoplax adhaerens (Tad), Lottia gigantea (Lgi), Daphnia pulex (Dpu), Caenorhabditis elegans (Cel), Homo sapiens (Hsa). Species names providing reference transcriptomes are abbreviated as per the following: Symbiodinium microadriaticum strain Kb8 (SmicKb8), Symbiodinium minutum strain Mf1.05b (SminMf1.05b), Symbiodinium kawagutii (Skaw.TS), Karenia brevis strain SP1 (KbrevSP1), Lingulodinium polyedrum (Lingu), Prorocentrum minimum (Proro), Amphidinium carterae (Amp), and Crypthecodinium cohnii (Crypt). A complete list of pfam domains and pfam annotations for all analyses are accessible in the supplement (Dataset S1.2, Dataset S1.3, Dataset S.14, Supplemental Information, Table S5).
Figure 3
Figure 3
Maximum-likelihood trees (1,000 bootstraps) for (A) bicarbonate transporters (PF00955 HCO3_cotransp) and (B) ammonium transporters (PF00909 Ammonium_transp), present in the genomes of Symbiodinium microadriaticum, Symbiodinium minutum, Symbiodinium kawagutii and the transcriptomes of Karenia brevis, Lingulodinium polyedrum, Amphidinium carterae, Crypthecodinium cohnii, and Prorocentrum minimum. Phylogenetic grouping of bicarbonate and ammonium transporters by species indicates lineage specific duplications in all dinoflagellate species. Only genes and transcripts with transporter domains with e-values > 10−15 and lengths above 150 amino acids were selected for the analysis. Species-specific gene duplications are colored according to species and edges with bootstrap support below 50 are collapsed. Files for phylogenetic tress are provided in the supplement (Supplemental Information, File S1 and File S2).
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References

    1. Taylor F. J. R. The biology of dinoflagellates. (1987).
    1. Lin S. Genomic understanding of dinoflagellates. Res. Microbiol. 162, 551–569, doi: 10.1016/j.resmic.2011.04.006 (2011). - DOI - PubMed
    1. Hackett J. D., Anderson D. M., Erdner D. L. & Bhattacharya D. Dinoflagellates: a remarkable evolutionary experiment. Am. J. Bot. 91, 1523–1534, doi: 10.3732/ajb.91.10.1523 (2004). - DOI - PubMed
    1. Wisecaver J. H., Brosnahan M. L. & Hackett J. D. Horizontal gene transfer is a significant driver of gene innovation in dinoflagellates. Genome Biol. Evol. 5, 2368–2381, doi: 10.1093/gbe/evt179 (2013). - DOI - PMC - PubMed
    1. Moustafa A. et al.. Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence. PLoS One 5, e9688 (2010). - PMC - PubMed

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