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Positive Selection of a Starch Synthesis Gene and Phenotypic Differentiation of Starch Accumulation in Symbiotic and Free-Living Coral Symbiont Dinoflagellate Species
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Abstract
Symbiosis is a basis for species diversification through interactions between organisms. In tropical and subtropical oceans, dinoflagellate symbionts belonging to the family Symbiodiniaceae, including the genus Symbiodinium, support the flourishment of cnidarian hosts, including corals, and thereby the ecology of oligotrophic oceans through their photosynthate carbon transfers. Although the genus Symbiodinium includes both free-living and symbiotic species, the detailed genetic background of their lifestyle differences remains unclear. In this study, we identified candidate genes involved in the evolutionary acquisition or maintenance of symbiosis in Symbiodinium spp. by detecting genes that have undergone positive selection during symbiotic and free-living lifestyle diversification. Using multiple Symbiodinium genomes to detect positive selection, 35 genes were identified, including a gene encoding soluble starch synthase SSY1 and genes related to metabolite secretion, which may be preferred for symbiotic lifestyles. In particular, our in silico analyses revealed that the SSY1 gene family has undergone extensive gene duplications in an ancestral dinoflagellate, and that the mutations detected as positive selection have occurred in the intrinsically disordered region of one of the homologs. Consistent with molecular evolution, the phenotypes of intracellular starch synthesis/accumulation were distinct between the symbiotic and free-living species of Symbiodinium when cultured under different pH and nitrogen conditions. These results provide molecular and phenotypic insights into symbiotic Symbiodinium-coral relationships.
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Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
OrthoFinder: phylogenetic orthology inference for comparative genomics
Emms, D. M., & Kelly, S. (2019) · Genome Biology · doi:10.1186/s13059-019-1832-y · Cited by 7,676
Keeling, P. J., Burki, F., Wilcox, H. M., Allam, B., Allen, E. E., Amaral-Zettler, L. A., Armbrust, E. V., Archibald, J. M., Bharti, A. K., Bell, C. J., et al. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001889 · Cited by 1,042
Flagged first, then by citations
Research works printed but not linked: 88
- Aranda, 2016, Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle, Sci Rep, 6, 39734, 10.1038/srep39734 · DOI
- Armstrong, 2018, Symbiont photosynthesis in giant clams is promoted by V-type H+-ATPase from host cells, J Exp Biol, 221, jeb177220, 10.1242/jeb.177220 · DOI
- Bachvaroff, 2008, From stop to start: tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae, PLoS One, 3, e2929, 10.1371/journal.pone.0002929 · DOI
- Baker, 2003, Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium, Annu Rev Ecol Evol Syst, 34, 661, 10.1146/annurev.ecolsys.34.011802.132417 · DOI
- Barott, 2015, Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis, Proc Natl Acad Sci U S A, 112, 607, 10.1073/pnas.1413483112 · DOI
- Baumgarten, 2015, The genome of Aiptasia, a sea anemone model for coral symbiosis, Proc Natl Acad Sci U S A, 112, 11893, 10.1073/pnas.1513318112 · DOI
- Blackall, 2015, Coral—the world's most diverse symbiotic ecosystem, Mol Ecol, 24, 5330, 10.1111/mec.13400 · DOI
- Bürgy, 2021, Coalescence and directed anisotropic growth of starch granule initials in subdomains of Arabidopsis thaliana chloroplasts, Nat Commun, 12, 6944, 10.1038/s41467-021-27151-5 · DOI
- Burriesci, 2012, Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis, J Exp Biol, 215, 3467, 10.1242/jeb.070946 · DOI
- Capella-Gutiérrez, 2009, Trimal: a tool for automated alignment trimming in large-scale phylogenetic analyses, Bioinformatics, 25, 1972, 10.1093/bioinformatics/btp348 · DOI
- Chen, 2018, Structural dissection of sterol glycosyltransferase UGT51 from Saccharomyces cerevisiae for substrate specificity, J Struct Biol, 204, 371, 10.1016/j.jsb.2018.11.001 · DOI
- Chen, 2018, Fastp: an ultra-fast all-in-one FASTQ preprocessor, Bioinformatics, 34, i884, 10.1093/bioinformatics/bty560 · DOI · Paper page
- Cheng, 2012, Diversification of genes encoding granule-bound starch synthase in monocots and dicots is marked by multiple genome-wide duplication events, PLoS One, 7, e30088, 10.1371/journal.pone.0030088 · DOI
- Costa, 2019, 10.17504/protocols.io.87khzkw · DOI
- Cui, 2023, Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia, Sci Adv, 9, eadf7108, 10.1126/sciadv.adf7108 · DOI
- Dauvillée, 2009, Genetic dissection of floridean starch synthesis in the cytosol of the model dinoflagellate Crypthecodinium cohnii, Proc Natl Acad Sci U S A, 106, 21126, 10.1073/pnas.0907424106 · DOI
- Davy, 2012, Cell biology of cnidarian-dinoflagellate symbiosis, Microbiol Mol Biol Rev, 76, 229, 10.1128/MMBR.05014-11 · DOI
- Dimijian, 2000, Evolving together: the biology of symbiosis, part 1, Proc (Bayl Univ Med Cent), 13, 217, 10.1080/08998280.2000.11927678 · DOI
- Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 · DOI · Paper page
- Finn, 2011, HMMER web server: interactive sequence similarity searching, Nucleic Acids Res, 39, W29, 10.1093/nar/gkr367 · DOI · Paper page
- Frankowiak, 2016, Photosymbiosis and the expansion of shallow-water corals, Sci Adv, 2, e1601122, 10.1126/sciadv.1601122 · DOI
- Gilbert, 2012, A symbiotic view of life: we have never been individuals, Q Rev Biol, 87, 325, 10.1086/668166 · DOI
- Gómez, 2012, A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata. Alveolata), Syst Biodivers, 10, 267, 10.1080/14772000.2012.721021 · DOI
- González-Pech, 2021, Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium, BMC Biol, 19, 73, 10.1186/s12915-021-00994-6 · DOI
- González-Pech, Genome assemblies and the associated annotations for seven Symbiodinium isolates, 10.14264/f1b3a11 · DOI
- González-Pech, 2017, Signatures of adaptation and symbiosis in genomes and transcriptomes of Symbiodinium, Sci Rep, 7, 15021, 10.1038/s41598-017-15029-w · DOI
- Gordon, 2010, Symbiodinium—invertebrate symbioses and the role of metabolomics, Mar Drugs, 8, 2546, 10.3390/md8102546 · DOI
- Grant, 2006, A cell signal from the coral Plesiastrea versipora reduces starch synthesis in its symbiotic alga, Symbiodinium sp, Comp Biochem Physiol A Comp Physiol, 144, 458, 10.1016/j.cbpa.2006.04.012 · DOI
- Granum, 2002, Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion, Mar Ecol Prog Ser, 242, 83, 10.3354/meps242083 · DOI
- Guillard, 1975, Culture of marine invertebrate animals, 29, 10.1007/978-1-4615-8714-9_3 · DOI
- Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis, Nat Protoc, 8, 1494, 10.1038/nprot.2013.084 · DOI · Paper page
- Hambleton, 2019, Sterol transfer by atypical cholesterol-binding NPC2 proteins in coral-algal symbiosis, eLife, 8, e43923, 10.7554/eLife.43923 · DOI
- Hansen, 2009, Symbiodinium natans sp. nov.: a “free-living” dinoflagellate from tenerife (northeast-Atlantic Ocean)(1), J Phycol, 45, 251, 10.1111/j.1529-8817.2008.00621.x · DOI
- Holehouse, 2024, The molecular basis for cellular function of intrinsically disordered protein regions, Nat Rev Mol Cell Biol, 25, 187, 10.1038/s41580-023-00673-0 · DOI
- Huerta-Cepas, 2016, ETE 3: reconstruction, analysis, and visualization of phylogenomic data, Mol Biol Evol, 33, 1635, 10.1093/molbev/msw046 · DOI
- Ishii, 2018, Isolation of uracil auxotroph mutants of coral symbiont alga for symbiosis studies, Sci Rep, 8, 3237, 10.1038/s41598-018-21499-3 · DOI
- Ishii, 2019, Global shifts in gene expression profiles accompanied with environmental changes in cnidarian-dinoflagellate endosymbiosis, G3-Genes Genom Genet, 9, 2337, 10.1534/g3.118.201012 · DOI
- Ishii, 2023, Environmental pH signals the release of monosaccharides from cell wall in coral symbiotic alga Tessmar-Raible, K & Schuman, MC, editors, eLife, 12, e80628, 10.7554/eLife.80628 · DOI
- Jacobovitz, 2021, Dinoflagellate symbionts escape vomocytosis by host cell immune suppression, Nat Microbiol, 6, 769, 10.1038/s41564-021-00897-w · DOI
- Janouškovec, 2017, Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics, Proc Natl Acad Sci U S A, 114, E171, 10.1073/pnas.1614842114 · DOI · Paper page
- Juergens, 2015, The regulation of photosynthetic structure and function during nitrogen deprivation in Chlamydomonas reinhardtii, Plant Physiol, 167, 558, 10.1104/pp.114.250530 · DOI
- Kalyaanamoorthy, 2017, ModelFinder: fast model selection for accurate phylogenetic estimates, Nat Methods, 14, 587, 10.1038/nmeth.4285 · DOI · Paper page
- LaJeunesse, 2018, Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts, Curr Biol, 28, 2570, 10.1016/j.cub.2018.07.008 · DOI
- Li, 2011, RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome, BMC Bioinform, 12, 323, 10.1186/1471-2105-12-323 · DOI · Paper page
- Li, 2006, Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences, Bioinformatics, 22, 1658, 10.1093/bioinformatics/btl158 · DOI
- Lin, 2015, The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis, Science, 350, 691, 10.1126/science.aad0408 · DOI
- Lin, 2024, A decade of dinoflagellate genomics illuminating an enigmatic eukaryote cell, BMC Genomics, 25, 932, 10.1186/s12864-024-10847-5 · DOI
- Liu, 2018, Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis, Commun Biol, 1, 95, 10.1038/s42003-018-0098-3 · DOI
- Löytynoja, 2005, An algorithm for progressive multiple alignment of sequences with insertions, Proc Natl Acad Sci U S A, 102, 10557, 10.1073/pnas.0409137102 · DOI
- Lu, 2020, Clade-specific sterol metabolites in dinoflagellate endosymbionts are associated with coral bleaching in response to environmental cues, mSystems, 5, e00765-20, 10.1128/mSystems.00765-20 · DOI
- Maor-Landaw, 2023, A candidate transporter allowing symbiotic dinoflagellates to feed their coral hosts, ISME Commun, 3, 1, 10.1038/s43705-023-00218-8 · DOI
- Maor-Landaw, 2020, Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae), Ecol Evol, 10, 451, 10.1002/ece3.5910 · DOI
- Maruyama, 2011, Eukaryote-to-eukaryote gene transfer gives rise to genome mosaicism in euglenids, BMC Evol Biol, 11, 105, 10.1186/1471-2148-11-105 · DOI
- Mashini, 2022, Immunolocalization of metabolite transporter proteins in a model cnidarian-dinoflagellate symbiosis, Appl Environ Microbiol, 88, e00412-22, 10.1128/aem.00412-22 · DOI
- McFall-Ngai, 2013, Animals in a bacterial world, a new imperative for the life sciences, Proc Natl Acad Sci U S A, 110, 3229, 10.1073/pnas.1218525110 · DOI
- Mies, 2017, Marine invertebrate larvae associated with Symbiodinium: a mutualism from the start?, Front Ecol Evol, 5, 56, 10.3389/fevo.2017.00056 · DOI
- Murakami-Murofushi, 1989, Expression of UDP-glucose: poriferasterol glucosyltransferase in the process of differentiation of a true slime mold, Physarum polycephalum, Biochim Biophys Acta, 992, 412, 10.1016/0304-4165(89)90108-6 · DOI
- Muscatine, 1990, Ecosystems of the world. Coral reefs, 75
- Nakamura, 2005, Some cyanobacteria synthesize semi-amylopectin type α-polyglucans instead of glycogen, Plant Cell Physiol, 46, 539, 10.1093/pcp/pci045 · DOI
- Necci, 2021, MobiDB-lite 3.0: fast consensus annotation of intrinsic disorder flavors in proteins, Bioinformatics, 36, 5533, 10.1093/bioinformatics/btaa1045 · DOI
- Nguyen, 2015, IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol Biol Evol, 32, 268, 10.1093/molbev/msu300 · DOI · Paper page
- Norton, 1992, The zooxanthellal tubular system in the giant clam, Biol Bull, 183, 503, 10.2307/1542028 · DOI
- Nougué, 2014, Molecular evolution accompanying functional divergence of duplicated genes along the plant starch biosynthesis pathway, BMC Evol Biol, 14, 103, 10.1186/1471-2148-14-103 · DOI
- Quigley, 2017, Temperature and water quality-related patterns in sediment-associated Symbiodinium communities impact symbiont uptake and fitness of juveniles in the genus Acropora, Front Mar Sci, 4, 401, 10.3389/fmars.2017.00401 · DOI
- Rädecker, 2021, Heat stress destabilizes symbiotic nutrient cycling in corals, Proc Natl Acad Sci U S A, 118, e2022653118, 10.1073/pnas.2022653118 · DOI
- Ral, 2006, Circadian clock regulation of starch metabolism establishes GBSSI as a major contributor to amylopectin synthesis in Chlamydomonas reinhardtii, Plant Physiol, 142, 305, 10.1104/pp.106.081885 · DOI
- Roth, 2014, The engine of the reef: photobiology of the coral-algal symbiosis, Front Microbiol, 22, 422, 10.3389/fmicb.2014.00422 · DOI
- Schneider, 2012, NIH image to ImageJ: 25 years of image analysis, Nat Methods, 9, 671, 10.1038/nmeth.2089 · DOI · Paper page
- Shimamura, 2020, Structure, metabolism and biological functions of steryl glycosides in mammals, Biochem J, 477, 4243, 10.1042/BCJ20200532 · DOI
- Shimonaga, 2008, Variation in storage α-glucans of the Porphyridiales (Rhodophyta), Plant Cell Physiol, 49, 103, 10.1093/pcp/pcm172 · DOI
- Shoguchi, 2013, Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure, Curr Biol, 23, 1399, 10.1016/j.cub.2013.05.062 · DOI
- Shoguchi, 2018, Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes, BMC Genomics, 19, 458, 10.1186/s12864-018-4857-9 · DOI
- Shoguchi, 2021, Gene clusters for biosynthesis of mycosporine-like amino acids in dinoflagellate nuclear genomes: possible recent horizontal gene transfer between species of Symbiodiniaceae (Dinophyceae), J Phycol, 58, 1, 10.1111/jpy.13219 · DOI
- Simpson, 2011, Evolutionary diversification of reef corals: a comparison of the molecular and fossil records, Evolution, 65, 3274, 10.1111/j.1558-5646.2011.01365.x · DOI
- Smith, 2015, Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection, Mol Biol Evol, 32, 1342, 10.1093/molbev/msv022 · DOI
- Sproles, 2018, Phylogenetic characterization of transporter proteins in the cnidarian-dinoflagellate symbiosis, Mol Phylogenet Evol, 120, 307, 10.1016/j.ympev.2017.12.007 · DOI
- Stephens, 2020, Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions, BMC Biol, 18, 1, 10.1186/s12915-020-00782-8 · DOI
- Storey, 2002, A direct approach to false discovery rates, J R Stat Soc Series B Stat Methodol, 64, 479, 10.1111/1467-9868.00346 · DOI · Paper page
- Szakacs, 2020, An inventory of lysosomal ABC transporters, FEBS Lett, 594, 3965, 10.1002/1873-3468.13967 · DOI
- Tetlow, 2020, A review of starch biosynthesis in relation to the building block-backbone model, Int J Mol Sci, 21, 7011, 10.3390/ijms21197011 · DOI
- Voolstra, 2015, The ReFuGe 2020 consortium—using “omics” approaches to explore the adaptability and resilience of coral holobionts to environmental change, Front Mar Sci, 2, 68, 10.3389/fmars.2015.00068 · DOI
- Warnecke, 1999, Cloning and functional expression of UGT genes encoding sterol glucosyltransferases from Saccharomyces cerevisiae, Candida albicans, Pichia pastoris, and Dictyostelium discoideum, J Biol Chem, 274, 13048, 10.1074/jbc.274.19.13048 · DOI
- Weng, 2014, Nitrogen deprivation induces lipid droplet accumulation and alters fatty acid metabolism in symbiotic dinoflagellates isolated from Aiptasia pulchella, Sci Rep, 4, 5777, 10.1038/srep05777 · DOI
- Xiang, 2020, Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations, Nat Commun, 11, 108, 10.1038/s41467-019-13963-z · DOI
- Yang, 2007, PAML 4: phylogenetic analysis by maximum likelihood, Mol Biol Evol, 24, 1586, 10.1093/molbev/msm088 · DOI · Paper page
- Yellowlees, 2008, Metabolic interactions between algal symbionts and invertebrate hosts, Plant Cell Environ, 31, 679, 10.1111/j.1365-3040.2008.01802.x · DOI
- Yorifuji, 2021, Unique environmental Symbiodiniaceae diversity at an isolated island in the northwestern Pacific, Mol Phylogenet Evol, 161, 107158, 10.1016/j.ympev.2021.107158 · DOI
- Yu, 2018, Characterization of steryl glycosides in marine microalgae by gas chromatography–triple quadrupole mass spectrometry (GC–QQQ-MS), J Sci Food Agric, 98, 1574, 10.1002/jsfa.8629 · DOI
Metadata
- Authors
- Ishii, Y., Kanamori, S., Deguchi, R., Kawata, M., Maruyama, S., Yoshida, T., & Kamikawa, R.
- Affiliations
- Kyoto University (JP)
- Tohoku University (JP)
- Miyagi University of Education (JP)
- The University of Tokyo (JP)
- Corresponding author
- Ishii, Yuu
- Maruyama, Shinichiro
- Kamikawa, Ryoma
- ORCID
- Venue
- Genome Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2025-07
- Volume
- 17
- Issue
- 7
- ISSN
- 1759-6653 (ISSN-L)
- PMC
- PMC12284398
- OpenAlex
- W4411965598
- Cited by
- 2
- References
- 3
- Citations by year
- 2026: 1 · 2025: 1
- FWCI
- 1.06
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Genome Biology and Evolution (publishedVersion, cc-by-nc)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- Kyoto University Research Information Repository (Kyoto University) (submittedVersion, cc-by-nc)
- Funders
- JSPS KAKENHI (20K15871, 23KJ2228, 24K18190, 23K23960, 23H04962, 24H01462, 24K21929, 25K02334, 21H05057)
- Starch Technologies Co., Ltd
- Topics
- Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Keywords
- Symbiodinium, zooxanthellae, coral symbiosis, positive selection, starch accumulation, gene duplication, intrinsically disordered regions, metabolite secretion, coral-algal symbiosis
- MeSH terms
- Animals, Dinoflagellida, Phenotype, Phylogeny, Selection, Genetic, Starch, Starch Synthase, Symbiosis, Evolution, Molecular, Anthozoa
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