Microbial Shift in the Enteric Bacteriome of Coral Reef Fish Following Climate-Driven Regime Shifts
Replacement of coral by macroalgae in post-disturbance reefs, also called a “coral-macroalgal regime shift”, is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect...
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Published in | Microorganisms (Basel) Vol. 9; no. 8; p. 1711 |
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Language | English |
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Abstract | Replacement of coral by macroalgae in post-disturbance reefs, also called a “coral-macroalgal regime shift”, is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coral-macroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria (Rikenella, Akkermensia, Desulfovibrio, Brachyspira) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions. |
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AbstractList | Replacement of coral by macroalgae in post-disturbance reefs, also called a "coralmacroalgal regime shift", is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coralmacroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria (Rikenella, Akkermensia, Desulfovibrio, Brachyspira) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions. Replacement of coral by macroalgae in post-disturbance reefs, also called a “coral-macroalgal regime shift”, is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coral-macroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria (Rikenella, Akkermensia, Desulfovibrio, Brachyspira) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions. Replacement of coral by macroalgae in post-disturbance reefs, also called a "coral-macroalgal regime shift", is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coral-macroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria (Rikenella, Akkermensia, Desulfovibrio, Brachyspira) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions.Replacement of coral by macroalgae in post-disturbance reefs, also called a "coral-macroalgal regime shift", is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coral-macroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria (Rikenella, Akkermensia, Desulfovibrio, Brachyspira) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions. Replacement of coral by macroalgae in post-disturbance reefs, also called a “coral-macroalgal regime shift”, is increasing in response to climate-driven ocean warming. Such ecosystem change is known to impact planktonic and benthic reef microbial communities but few studies have examined the effect on animal microbiota. In order to understand the consequence of coral-macroalgal shifts on the coral reef fish enteric bacteriome, we used a metabarcoding approach to examine the gut bacteriomes of 99 individual fish representing 36 species collected on reefs of the Inner Seychelles islands that, following bleaching, had either recovered to coral domination, or shifted to macroalgae. While the coral-macroalgal shift did not influence the diversity, richness or variability of fish gut bacteriomes, we observed a significant effect on the composition (R2 = 0.02; p = 0.001), especially in herbivorous fishes (R2 = 0.07; p = 0.001). This change is accompanied by a significant increase in the proportion of fermentative bacteria ( Rikenella, Akkermensia , Desulfovibrio , Brachyspira ) and associated metabolisms (carbohydrates metabolism, DNA replication, and nitrogen metabolism) in relation to the strong turnover of Scarinae and Siganidae fishes. Predominance of fermentative metabolisms in fish found on macroalgal dominated reefs indicates that regime shifts not only affect the taxonomic composition of fish bacteriomes, but also have the potential to affect ecosystem functioning through microbial functions. |
Author | Restrepo, Claudia Ximena Ortiz Hicks, Christina C. Bouvier, Thierry Robinson, James P. W. Graham, Nicholas A. J. Marconnet, Clémence Auguet, Jean-Christophe Cheutin, Marie-Charlotte Villéger, Sébastien Bettarel, Yvan |
AuthorAffiliation | 2 Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK; christina.hicks@lancaster.ac.uk (C.C.H.); james.robinson@lancaster.ac.uk (J.P.W.R.); nick.graham@lancaster.ac.uk (N.A.J.G.) 1 UMR MARBEC, Université de Montpellier, CNRS, Ifremer, IRD, 34095 Montpellier, France; sebastien.villeger@cnrs.fr (S.V.); marconnet.clemence@gmail.com (C.M.); claudiaximenaro@gmail.com (C.X.O.R.); yvan.bettarel@ird.fr (Y.B.); thierry.bouvier@cnrs.fr (T.B.); Jean-christophe.AUGUET@cnrs.fr (J.-C.A.) |
AuthorAffiliation_xml | – name: 1 UMR MARBEC, Université de Montpellier, CNRS, Ifremer, IRD, 34095 Montpellier, France; sebastien.villeger@cnrs.fr (S.V.); marconnet.clemence@gmail.com (C.M.); claudiaximenaro@gmail.com (C.X.O.R.); yvan.bettarel@ird.fr (Y.B.); thierry.bouvier@cnrs.fr (T.B.); Jean-christophe.AUGUET@cnrs.fr (J.-C.A.) – name: 2 Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK; christina.hicks@lancaster.ac.uk (C.C.H.); james.robinson@lancaster.ac.uk (J.P.W.R.); nick.graham@lancaster.ac.uk (N.A.J.G.) |
Author_xml | – sequence: 1 givenname: Marie-Charlotte orcidid: 0000-0001-7711-7512 surname: Cheutin fullname: Cheutin, Marie-Charlotte – sequence: 2 givenname: Sébastien surname: Villéger fullname: Villéger, Sébastien – sequence: 3 givenname: Christina C. surname: Hicks fullname: Hicks, Christina C. – sequence: 4 givenname: James P. W. orcidid: 0000-0002-7614-1112 surname: Robinson fullname: Robinson, James P. W. – sequence: 5 givenname: Nicholas A. J. surname: Graham fullname: Graham, Nicholas A. J. – sequence: 6 givenname: Clémence surname: Marconnet fullname: Marconnet, Clémence – sequence: 7 givenname: Claudia Ximena Ortiz surname: Restrepo fullname: Restrepo, Claudia Ximena Ortiz – sequence: 8 givenname: Yvan surname: Bettarel fullname: Bettarel, Yvan – sequence: 9 givenname: Thierry surname: Bouvier fullname: Bouvier, Thierry – sequence: 10 givenname: Jean-Christophe surname: Auguet fullname: Auguet, Jean-Christophe |
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CitedBy_id | crossref_primary_10_3389_fmicb_2022_963456 crossref_primary_10_1016_j_marpolbul_2023_115267 crossref_primary_10_1007_s00227_022_04098_9 crossref_primary_10_1186_s12866_022_02709_5 crossref_primary_10_1186_s12866_024_03698_3 crossref_primary_10_24072_pcjournal_446 crossref_primary_10_3389_fmicb_2022_906299 crossref_primary_10_1007_s00248_024_02423_x |
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Copyright | 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Distributed under a Creative Commons Attribution 4.0 International License 2021 by the authors. 2021 |
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Snippet | Replacement of coral by macroalgae in post-disturbance reefs, also called a “coral-macroalgal regime shift”, is increasing in response to climate-driven ocean... Replacement of coral by macroalgae in post-disturbance reefs, also called a "coral-macroalgal regime shift", is increasing in response to climate-driven ocean... Replacement of coral by macroalgae in post-disturbance reefs, also called a "coralmacroalgal regime shift", is increasing in response to climate-driven ocean... |
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SubjectTerms | Algae Animals bacteriome barcoding Bleaching Brachyspira Carbohydrates Composition effects coral reef fish Coral reefs coral-macroalgal shift corals Desulfovibrio digestive system DNA barcoding DNA biosynthesis DNA replication Ecological function ecosystems enteric bacteriome Environmental changes Environmental Sciences Fish Fishing Gene amplification Herbivorous fish Laboratories macroalgae Marine ecosystems Microbial activity microbial functions Microbiota Microorganisms Nitrogen metabolism Ocean temperature Ocean warming plankton Reef fish Rikenella Seychelles Siganidae Taxonomy |
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Title | Microbial Shift in the Enteric Bacteriome of Coral Reef Fish Following Climate-Driven Regime Shifts |
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