Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome

Coral bleaching, i.e., the loss of photosynthetic algal endosymbionts, caused by ocean warming is now among the main factors driving global reef decline, making the elucidation of factors that contribute to thermotolerance important. Recent studies implicate high salinity as a contributing factor in...

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Main Authors: Janna L. Randle, Anny Cárdenas, Hagen M. Gegner, Maren Ziegler, Christian R. Voolstra
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-11-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2020.573635/full
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author Janna L. Randle
Anny Cárdenas
Anny Cárdenas
Hagen M. Gegner
Hagen M. Gegner
Maren Ziegler
Maren Ziegler
Christian R. Voolstra
Christian R. Voolstra
author_facet Janna L. Randle
Anny Cárdenas
Anny Cárdenas
Hagen M. Gegner
Hagen M. Gegner
Maren Ziegler
Maren Ziegler
Christian R. Voolstra
Christian R. Voolstra
author_sort Janna L. Randle
collection DOAJ
description Coral bleaching, i.e., the loss of photosynthetic algal endosymbionts, caused by ocean warming is now among the main factors driving global reef decline, making the elucidation of factors that contribute to thermotolerance important. Recent studies implicate high salinity as a contributing factor in cnidarians, potentially explaining the high thermotolerance of corals from the Arabian Seas. Here we characterized bacterial community composition under heat stress at different salinities using the coral model Aiptasia. Exposure of two Aiptasia host-algal symbiont pairings (H2-SSB01 and CC7-SSA01) to ambient (25°C) and heat stress (34°C) temperatures at low (36 PSU), intermediate (39 PSU), and high (42 PSU) salinities showed that bacterial community composition at high salinity was significantly different, concomitant with reduced bleaching susceptibility in H2-SSB01, not observed in CC7-SSA01. Elucidation of bacteria that showed increased relative abundance at high salinity, irrespective of heat stress, revealed candidate taxa that could potentially contribute to the observed increased thermotolerance. We identified 4 (H2-SSB01) and 3 (CC7-SSA01) bacterial taxa belonging to the orders Alteromonadales (1 OTU), Oligoflexales (1 OTU), Rhizobiales (2 OTUs), and Rhodobacterales (2 OTUs), suggesting that only few bacterial taxa are potential contributors to an increase in thermal tolerance at high salinities. These taxa have previously been implicated in nitrogen and DMSP cycling, processes that are considered to affect thermotolerance. Our study demonstrates microbiome restructuring in symbiotic cnidarians under heat stress at different salinities. As such, it underlines how host-associated bacterial communities adapt to prevailing environmental conditions with putative consequences for the environmental stress tolerance of the emergent metaorganism.
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spelling doaj.art-da027b507c69471c850b7018e1a9a6572022-12-21T22:09:07ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452020-11-01710.3389/fmars.2020.573635573635Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial MicrobiomeJanna L. Randle0Anny Cárdenas1Anny Cárdenas2Hagen M. Gegner3Hagen M. Gegner4Maren Ziegler5Maren Ziegler6Christian R. Voolstra7Christian R. Voolstra8Division of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaDivision of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaDepartment of Biology, University of Konstanz, Konstanz, GermanyDivision of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaCentre for Organismal Studies, University of Heidelberg, Heidelberg, GermanyDivision of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaDepartment of Animal Ecology and Systematics, Justus Liebig University Giessen, Giessen, GermanyDivision of Biological and Environmental Science and Engineering, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi ArabiaDepartment of Biology, University of Konstanz, Konstanz, GermanyCoral bleaching, i.e., the loss of photosynthetic algal endosymbionts, caused by ocean warming is now among the main factors driving global reef decline, making the elucidation of factors that contribute to thermotolerance important. Recent studies implicate high salinity as a contributing factor in cnidarians, potentially explaining the high thermotolerance of corals from the Arabian Seas. Here we characterized bacterial community composition under heat stress at different salinities using the coral model Aiptasia. Exposure of two Aiptasia host-algal symbiont pairings (H2-SSB01 and CC7-SSA01) to ambient (25°C) and heat stress (34°C) temperatures at low (36 PSU), intermediate (39 PSU), and high (42 PSU) salinities showed that bacterial community composition at high salinity was significantly different, concomitant with reduced bleaching susceptibility in H2-SSB01, not observed in CC7-SSA01. Elucidation of bacteria that showed increased relative abundance at high salinity, irrespective of heat stress, revealed candidate taxa that could potentially contribute to the observed increased thermotolerance. We identified 4 (H2-SSB01) and 3 (CC7-SSA01) bacterial taxa belonging to the orders Alteromonadales (1 OTU), Oligoflexales (1 OTU), Rhizobiales (2 OTUs), and Rhodobacterales (2 OTUs), suggesting that only few bacterial taxa are potential contributors to an increase in thermal tolerance at high salinities. These taxa have previously been implicated in nitrogen and DMSP cycling, processes that are considered to affect thermotolerance. Our study demonstrates microbiome restructuring in symbiotic cnidarians under heat stress at different salinities. As such, it underlines how host-associated bacterial communities adapt to prevailing environmental conditions with putative consequences for the environmental stress tolerance of the emergent metaorganism.https://www.frontiersin.org/articles/10.3389/fmars.2020.573635/fullbacterial communityheat stresssalinityholobiontmetaorganismthermotolerance
spellingShingle Janna L. Randle
Anny Cárdenas
Anny Cárdenas
Hagen M. Gegner
Hagen M. Gegner
Maren Ziegler
Maren Ziegler
Christian R. Voolstra
Christian R. Voolstra
Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome
Frontiers in Marine Science
bacterial community
heat stress
salinity
holobiont
metaorganism
thermotolerance
title Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome
title_full Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome
title_fullStr Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome
title_full_unstemmed Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome
title_short Salinity-Conveyed Thermotolerance in the Coral Model Aiptasia Is Accompanied by Distinct Changes of the Bacterial Microbiome
title_sort salinity conveyed thermotolerance in the coral model aiptasia is accompanied by distinct changes of the bacterial microbiome
topic bacterial community
heat stress
salinity
holobiont
metaorganism
thermotolerance
url https://www.frontiersin.org/articles/10.3389/fmars.2020.573635/full
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