Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales

Handle URI:
http://hdl.handle.net/10754/615932
Title:
Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales
Authors:
Neave, Matthew J.; Rachmawati, Rita; Xun, Liping; Michell, Craig; Bourne, David G; Apprill, Amy; Voolstra, Christian R. ( 0000-0003-4555-3795 )
Abstract:
Reef-building corals are well regarded not only for their obligate association with endosymbiotic algae, but also with prokaryotic symbionts, the specificity of which remains elusive. To identify the central microbial symbionts of corals, their specificity across species and conservation over geographic regions, we sequenced partial SSU ribosomal RNA genes of Bacteria and Archaea from the common corals Stylophora pistillata and Pocillopora verrucosa across 28 reefs within seven major geographical regions. We demonstrate that both corals harbor Endozoicomonas bacteria as their prevalent symbiont. Importantly, catalyzed reporter deposition–fluorescence in situ hybridization (CARD–FISH) with Endozoicomonas-specific probes confirmed their residence as large aggregations deep within coral tissues. Using fine-scale genotyping techniques and single-cell genomics, we demonstrate that P. verrucosa harbors the same Endozoicomonas, whereas S. pistillata associates with geographically distinct genotypes. This specificity may be shaped by the different reproductive strategies of the hosts, potentially uncovering a pattern of symbiont selection that is linked to life history. Spawning corals such as P. verrucosa acquire prokaryotes from the environment. In contrast, brooding corals such as S. pistillata release symbiont-packed planula larvae, which may explain a strong regional signature in their microbiome. Our work contributes to the factors underlying microbiome specificity and adds detail to coral holobiont functioning.
KAUST Department:
Red Sea Research Center (RSRC); Biological and Environmental Sciences and Engineering (BESE) Division
Citation:
Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales 2016 The ISME Journal
Publisher:
Springer Nature
Journal:
The ISME Journal
Issue Date:
8-Jul-2016
DOI:
10.1038/ismej.2016.95
Type:
Article
ISSN:
1751-7362; 1751-7370
Sponsors:
We thank Ray Dalio for funding the Micronesian expedition and K Hughen, J Ossolinski, C Smith and A Santoro, and the crew of the M/V Alucia for sampling support and the Federated States of Micronesia for collection permits FM12-11-03S and FM12-11-05S. In American Samoa, we are grateful to T Clark of the National Park Service and the Department of Marine and Wildlife Resources for permitting (No. 001) coral collections. In the Maldives, we thank G Arlotti and the Korallion Laboratory for sampling support and the Ministry of Fisheries and Agriculture for collection permits (No. (OTHR)30-D/INDIV/2013/359). In Australia, we acknowledge M McCulloch and the University of Western Australia for sampling support and the Department of Parks and Wildlife, Western Australia, for permitting (Licence Number SF009558). For sampling in the Red Sea, we are grateful to the CMOR team at KAUST and Red Sea Dream Divers. In Indonesia, we thank P Barber, L Mathar, M Krey, M Dailami, A Fritts-Penniman, the Indonesian Biodiversity Research Center, S-Y Vanson Liu, MZI Noer and A Cahyadi for sampling support, and collection permits from the Wakatobi National Park and the Natural Resources Conservation Center in East Nusa Tenggara, Manokwari (West Papua) and Bali. We acknowledge K Selph of the UH SOEST flow cytometry facility for cell enumeration and J Jennings of Oregon State University for inorganic nutrient analysis. This research was supported by a KAUST-WHOI Post-doctoral Partnership Award to MN and a KAUST-WHOI Special Academic Partnership Funding Reserve Award to CRV and AA. Research in this study was further supported by baseline research funds to CRV by KAUST and NSF award OCE-1233612 to AA. RR was supported by the ct-PIRE Project, Robert Lemelson Fellowship, Graduate Research Award (UCLA), Women Divers Hall of Fame—Sister Fund Conservation Award and a Betty and E. P. Franklin Grant in Tropical Biology and Conservation. Many thanks to E Tambuttė and the Centre Scientifique de Monaco (CSM) for provision of coral polyp images. We thank the three anonymous referees for comments that improved this manuscript.
Additional Links:
http://www.nature.com/doifinder/10.1038/ismej.2016.95
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Full metadata record

DC FieldValue Language
dc.contributor.authorNeave, Matthew J.en
dc.contributor.authorRachmawati, Ritaen
dc.contributor.authorXun, Lipingen
dc.contributor.authorMichell, Craigen
dc.contributor.authorBourne, David Gen
dc.contributor.authorApprill, Amyen
dc.contributor.authorVoolstra, Christian R.en
dc.date.accessioned2016-07-11T10:01:29Z-
dc.date.available2016-07-11T10:01:29Z-
dc.date.issued2016-07-08-
dc.identifier.citationDifferential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales 2016 The ISME Journalen
dc.identifier.issn1751-7362-
dc.identifier.issn1751-7370-
dc.identifier.doi10.1038/ismej.2016.95-
dc.identifier.urihttp://hdl.handle.net/10754/615932-
dc.description.abstractReef-building corals are well regarded not only for their obligate association with endosymbiotic algae, but also with prokaryotic symbionts, the specificity of which remains elusive. To identify the central microbial symbionts of corals, their specificity across species and conservation over geographic regions, we sequenced partial SSU ribosomal RNA genes of Bacteria and Archaea from the common corals Stylophora pistillata and Pocillopora verrucosa across 28 reefs within seven major geographical regions. We demonstrate that both corals harbor Endozoicomonas bacteria as their prevalent symbiont. Importantly, catalyzed reporter deposition–fluorescence in situ hybridization (CARD–FISH) with Endozoicomonas-specific probes confirmed their residence as large aggregations deep within coral tissues. Using fine-scale genotyping techniques and single-cell genomics, we demonstrate that P. verrucosa harbors the same Endozoicomonas, whereas S. pistillata associates with geographically distinct genotypes. This specificity may be shaped by the different reproductive strategies of the hosts, potentially uncovering a pattern of symbiont selection that is linked to life history. Spawning corals such as P. verrucosa acquire prokaryotes from the environment. In contrast, brooding corals such as S. pistillata release symbiont-packed planula larvae, which may explain a strong regional signature in their microbiome. Our work contributes to the factors underlying microbiome specificity and adds detail to coral holobiont functioning.en
dc.description.sponsorshipWe thank Ray Dalio for funding the Micronesian expedition and K Hughen, J Ossolinski, C Smith and A Santoro, and the crew of the M/V Alucia for sampling support and the Federated States of Micronesia for collection permits FM12-11-03S and FM12-11-05S. In American Samoa, we are grateful to T Clark of the National Park Service and the Department of Marine and Wildlife Resources for permitting (No. 001) coral collections. In the Maldives, we thank G Arlotti and the Korallion Laboratory for sampling support and the Ministry of Fisheries and Agriculture for collection permits (No. (OTHR)30-D/INDIV/2013/359). In Australia, we acknowledge M McCulloch and the University of Western Australia for sampling support and the Department of Parks and Wildlife, Western Australia, for permitting (Licence Number SF009558). For sampling in the Red Sea, we are grateful to the CMOR team at KAUST and Red Sea Dream Divers. In Indonesia, we thank P Barber, L Mathar, M Krey, M Dailami, A Fritts-Penniman, the Indonesian Biodiversity Research Center, S-Y Vanson Liu, MZI Noer and A Cahyadi for sampling support, and collection permits from the Wakatobi National Park and the Natural Resources Conservation Center in East Nusa Tenggara, Manokwari (West Papua) and Bali. We acknowledge K Selph of the UH SOEST flow cytometry facility for cell enumeration and J Jennings of Oregon State University for inorganic nutrient analysis. This research was supported by a KAUST-WHOI Post-doctoral Partnership Award to MN and a KAUST-WHOI Special Academic Partnership Funding Reserve Award to CRV and AA. Research in this study was further supported by baseline research funds to CRV by KAUST and NSF award OCE-1233612 to AA. RR was supported by the ct-PIRE Project, Robert Lemelson Fellowship, Graduate Research Award (UCLA), Women Divers Hall of Fame—Sister Fund Conservation Award and a Betty and E. P. Franklin Grant in Tropical Biology and Conservation. Many thanks to E Tambuttė and the Centre Scientifique de Monaco (CSM) for provision of coral polyp images. We thank the three anonymous referees for comments that improved this manuscript.en
dc.language.isoenen
dc.publisherSpringer Natureen
dc.relation.urlhttp://www.nature.com/doifinder/10.1038/ismej.2016.95en
dc.rightsThis work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 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-nc-sa/4.0/.en
dc.titleDifferential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scalesen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.identifier.journalThe ISME Journalen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionMarine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USAen
dc.contributor.institutionDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USAen
dc.contributor.institutionAustralian Institute of Marine Science and College of Science and Engineering, James Cook University Townsville, Townsville, Queensland, Australiaen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorNeave, Matthew J.en
kaust.authorMichell, Craigen
kaust.authorVoolstra, Christian R.en
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