Comparative genomics explains the evolutionary success of reef-forming corals
Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2016-05-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/13288 |
| _version_ | 1811181079488364544 |
|---|---|
| author | Debashish Bhattacharya Shobhit Agrawal Manuel Aranda Sebastian Baumgarten Mahdi Belcaid Jeana L Drake Douglas Erwin Sylvian Foret Ruth D Gates David F Gruber Bishoy Kamel Michael P Lesser Oren Levy Yi Jin Liew Matthew MacManes Tali Mass Monica Medina Shaadi Mehr Eli Meyer Dana C Price Hollie M Putnam Huan Qiu Chuya Shinzato Eiichi Shoguchi Alexander J Stokes Sylvie Tambutté Dan Tchernov Christian R Voolstra Nicole Wagner Charles W Walker Andreas PM Weber Virginia Weis Ehud Zelzion Didier Zoccola Paul G Falkowski |
| author_facet | Debashish Bhattacharya Shobhit Agrawal Manuel Aranda Sebastian Baumgarten Mahdi Belcaid Jeana L Drake Douglas Erwin Sylvian Foret Ruth D Gates David F Gruber Bishoy Kamel Michael P Lesser Oren Levy Yi Jin Liew Matthew MacManes Tali Mass Monica Medina Shaadi Mehr Eli Meyer Dana C Price Hollie M Putnam Huan Qiu Chuya Shinzato Eiichi Shoguchi Alexander J Stokes Sylvie Tambutté Dan Tchernov Christian R Voolstra Nicole Wagner Charles W Walker Andreas PM Weber Virginia Weis Ehud Zelzion Didier Zoccola Paul G Falkowski |
| author_sort | Debashish Bhattacharya |
| collection | DOAJ |
| description | Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years. |
| first_indexed | 2024-04-11T09:13:46Z |
| format | Article |
| id | doaj.art-4eb7a71076b04ddf989766337bbf1faf |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:13:46Z |
| publishDate | 2016-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-4eb7a71076b04ddf989766337bbf1faf2022-12-22T04:32:26ZengeLife Sciences Publications LtdeLife2050-084X2016-05-01510.7554/eLife.13288Comparative genomics explains the evolutionary success of reef-forming coralsDebashish Bhattacharya0Shobhit Agrawal1Manuel Aranda2Sebastian Baumgarten3Mahdi Belcaid4Jeana L Drake5Douglas Erwin6Sylvian Foret7Ruth D Gates8David F Gruber9Bishoy Kamel10https://orcid.org/0000-0003-2934-3827Michael P Lesser11Oren Levy12Yi Jin Liew13Matthew MacManes14https://orcid.org/0000-0002-2368-6960Tali Mass15Monica Medina16Shaadi Mehr17Eli Meyer18Dana C Price19Hollie M Putnam20Huan Qiu21Chuya Shinzato22Eiichi Shoguchi23Alexander J Stokes24https://orcid.org/0000-0002-3526-4685Sylvie Tambutté25Dan Tchernov26Christian R Voolstra27https://orcid.org/0000-0003-4555-3795Nicole Wagner28Charles W Walker29Andreas PM Weber30Virginia Weis31Ehud Zelzion32Didier Zoccola33https://orcid.org/0000-0002-1524-8098Paul G Falkowski34https://orcid.org/0000-0002-2353-1969Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, United States; Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, United StatesRed Sea Research Center, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaRed Sea Research Center, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaRed Sea Research Center, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaHawaii Institute of Marine Biology, Kaneohe, United StatesEnvironmental Biophysics and Molecular Ecology Program, Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, United StatesSmithsonian Institution, National Museum of Natural History, Washington, United StatesARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Australia; Research School of Biology, Australian National University, Canberra, AustraliaHawaii Institute of Marine Biology, Kaneohe, United StatesAmerican Museum of Natural History, Sackler Institute for Comparative Genomics, New York, United States; Department of Natural Sciences, City University of New York, Baruch College and The Graduate Center, New York, United StatesDepartment of Biology, Mueller Lab, Penn State University, University Park, United StatesSchool of Marine Science and Ocean Engineering, University of New Hampshire, Durham, United StatesThe Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gam, IsraelRed Sea Research Center, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDepartment of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United StatesEnvironmental Biophysics and Molecular Ecology Program, Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, United States; Marine Biology Department, The Leon H. Charney School of Marine Sciences, University of Haifa, Mt. Carmel, IsraelDepartment of Biology, Mueller Lab, Penn State University, University Park, United StatesAmerican Museum of Natural History, Sackler Institute for Comparative Genomics, New York, United States; Biological Science Department, State University of New York, College at Old Westbury, New York, United StatesDepartment of Integrative Biology, Oregon State University, Corvallis, United StatesDepartment of Plant Biology and Pathology, Rutgers University, New Brunswick, United StatesHawaii Institute of Marine Biology, Kaneohe, United StatesDepartment of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, United StatesMarine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, JapanMarine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, JapanLaboratory of Experimental Medicine and Department of Cell and Molecular Biology, John A. Burns School of Medicine, Honolulu, United States; Chaminade University, Honolulu, United StatesCentre Scientifique de Monaco, Quai Antoine Ier, MonacoMarine Biology Department, The Leon H. Charney School of Marine Sciences, University of Haifa, Mt. Carmel, IsraelRed Sea Research Center, Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi ArabiaDepartment of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, United StatesDepartment of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, United StatesInstitute of Plant Biochemistry, Heinrich-Heine-Universität, Düsseldorf, GermanyDepartment of Integrative Biology, Oregon State University, Corvallis, United StatesDepartment of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, United StatesCentre Scientifique de Monaco, Quai Antoine Ier, MonacoEnvironmental Biophysics and Molecular Ecology Program, Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, United States; Department of Earth and Planetary Sciences, Rutgers University, New Jersey, United StatesTranscriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years.https://elifesciences.org/articles/13288coralsbiomineralizationstress responsesymbiosishorizontal gene transfer |
| spellingShingle | Debashish Bhattacharya Shobhit Agrawal Manuel Aranda Sebastian Baumgarten Mahdi Belcaid Jeana L Drake Douglas Erwin Sylvian Foret Ruth D Gates David F Gruber Bishoy Kamel Michael P Lesser Oren Levy Yi Jin Liew Matthew MacManes Tali Mass Monica Medina Shaadi Mehr Eli Meyer Dana C Price Hollie M Putnam Huan Qiu Chuya Shinzato Eiichi Shoguchi Alexander J Stokes Sylvie Tambutté Dan Tchernov Christian R Voolstra Nicole Wagner Charles W Walker Andreas PM Weber Virginia Weis Ehud Zelzion Didier Zoccola Paul G Falkowski Comparative genomics explains the evolutionary success of reef-forming corals eLife corals biomineralization stress response symbiosis horizontal gene transfer |
| title | Comparative genomics explains the evolutionary success of reef-forming corals |
| title_full | Comparative genomics explains the evolutionary success of reef-forming corals |
| title_fullStr | Comparative genomics explains the evolutionary success of reef-forming corals |
| title_full_unstemmed | Comparative genomics explains the evolutionary success of reef-forming corals |
| title_short | Comparative genomics explains the evolutionary success of reef-forming corals |
| title_sort | comparative genomics explains the evolutionary success of reef forming corals |
| topic | corals biomineralization stress response symbiosis horizontal gene transfer |
| url | https://elifesciences.org/articles/13288 |
| work_keys_str_mv | AT debashishbhattacharya comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT shobhitagrawal comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT manuelaranda comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT sebastianbaumgarten comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT mahdibelcaid comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT jeanaldrake comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT douglaserwin comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT sylvianforet comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT ruthdgates comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT davidfgruber comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT bishoykamel comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT michaelplesser comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT orenlevy comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT yijinliew comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT matthewmacmanes comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT talimass comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT monicamedina comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT shaadimehr comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT elimeyer comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT danacprice comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT holliemputnam comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT huanqiu comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT chuyashinzato comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT eiichishoguchi comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT alexanderjstokes comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT sylvietambutte comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT dantchernov comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT christianrvoolstra comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT nicolewagner comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT charleswwalker comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT andreaspmweber comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT virginiaweis comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT ehudzelzion comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT didierzoccola comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals AT paulgfalkowski comparativegenomicsexplainstheevolutionarysuccessofreefformingcorals |