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

Handle URI:
http://hdl.handle.net/10754/622071
Title:
Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle
Authors:
Aranda, Manuel ( 0000-0001-6673-016X ) ; Li, Yangyang ( 0000-0003-4469-0659 ) ; Liew, Yi Jin ( 0000-0003-2553-8870 ) ; Baumgarten, Sebastian ( 0000-0003-2646-7699 ) ; Simakov, O.; Wilson, M. C.; Piel, J.; Ashoor, Haitham ( 0000-0003-2527-0317 ) ; Bougouffa, Salim ( 0000-0001-9218-6452 ) ; Bajic, Vladimir B. ( 0000-0001-5435-4750 ) ; Ryu, Tae Woo; Ravasi, Timothy ( 0000-0002-9950-465X ) ; Bayer, Till; Micklem, G.; Kim, H.; Bhak, J.; LaJeunesse, T. C.; Voolstra, Christian R. ( 0000-0003-4555-3795 )
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.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Red Sea Research Center (RSRC); Computational Bioscience Research Center (CBRC); Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division; KAUST Environmental Epigenetics Research Program (KEEP)
Citation:
Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, et al. (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Scientific Reports 6: 39734. Available: http://dx.doi.org/10.1038/srep39734.
Publisher:
Springer Nature
Journal:
Scientific Reports
Issue Date:
22-Dec-2016
DOI:
10.1038/srep39734
Type:
Article
ISSN:
2045-2322
Sponsors:
We thank Matt E. Oates and Julian Gough for protein set annotation to Superfamily, and Adrian C. Carr for preliminary genome assembly. Research reported in this publication was supported by the King Abdullah University of Science and Technology (KAUST) and by an AEA2 grant to V.B.B., G.M., T.R., and C.R.V.
Additional Links:
http://www.nature.com/articles/srep39734
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Computational Bioscience Research Center (CBRC); Biological and Environmental Sciences and Engineering (BESE) Division; Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorAranda, Manuelen
dc.contributor.authorLi, Yangyangen
dc.contributor.authorLiew, Yi Jinen
dc.contributor.authorBaumgarten, Sebastianen
dc.contributor.authorSimakov, O.en
dc.contributor.authorWilson, M. C.en
dc.contributor.authorPiel, J.en
dc.contributor.authorAshoor, Haithamen
dc.contributor.authorBougouffa, Salimen
dc.contributor.authorBajic, Vladimir B.en
dc.contributor.authorRyu, Tae Wooen
dc.contributor.authorRavasi, Timothyen
dc.contributor.authorBayer, Tillen
dc.contributor.authorMicklem, G.en
dc.contributor.authorKim, H.en
dc.contributor.authorBhak, J.en
dc.contributor.authorLaJeunesse, T. C.en
dc.contributor.authorVoolstra, Christian R.en
dc.date.accessioned2016-12-26T13:42:26Z-
dc.date.available2016-12-26T13:42:26Z-
dc.date.issued2016-12-22en
dc.identifier.citationAranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, et al. (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Scientific Reports 6: 39734. Available: http://dx.doi.org/10.1038/srep39734.en
dc.identifier.issn2045-2322en
dc.identifier.doi10.1038/srep39734en
dc.identifier.urihttp://hdl.handle.net/10754/622071-
dc.description.abstractDespite 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.en
dc.description.sponsorshipWe thank Matt E. Oates and Julian Gough for protein set annotation to Superfamily, and Adrian C. Carr for preliminary genome assembly. Research reported in this publication was supported by the King Abdullah University of Science and Technology (KAUST) and by an AEA2 grant to V.B.B., G.M., T.R., and C.R.V.en
dc.publisherSpringer Natureen
dc.relation.urlhttp://www.nature.com/articles/srep39734en
dc.rightsThis work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleGenomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyleen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.contributor.departmentComputer, Electrical and Mathematical Sciences and Engineering (CEMSE) Divisionen
dc.contributor.departmentKAUST Environmental Epigenetics Research Program (KEEP)en
dc.identifier.journalScientific Reportsen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionCentre for Organismal Studies, Heidelberg University, 69120 Heidelberg, Germanyen
dc.contributor.institutionInstitute of Microbiology, Eidgenössische Technische Hochschule Zurich, Vladimir-Prelog-Weg 4, 8093 Zurich, Switzerlanden
dc.contributor.institutionGEOMAR Department: Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germanyen
dc.contributor.institutionDepartment of Genetics, University of Cambridge, Cambridge CB2 3EH, UKen
dc.contributor.institutionPersonal Genomics Institute, Genome Research Foundation, Suwon, Republic of Koreaen
dc.contributor.institutionDepartment of Biology, The Pennsylvania State University, University Park, PA 16802, USAen
kaust.authorAranda, Manuelen
kaust.authorLi, Yangyangen
kaust.authorLiew, Yi Jinen
kaust.authorBaumgarten, Sebastianen
kaust.authorAshoor, Haithamen
kaust.authorBougouffa, Salimen
kaust.authorBajic, Vladimir B.en
kaust.authorRyu, Tae Wooen
kaust.authorRavasi, Timothyen
kaust.authorBayer, Tillen
kaust.authorVoolstra, Christian R.en
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