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 inMicroorganisms (Basel) Vol. 9; no. 8; p. 1711
Main Authors Cheutin, Marie-Charlotte, Villéger, Sébastien, Hicks, Christina C., Robinson, James P. W., Graham, Nicholas A. J., Marconnet, Clémence, Restrepo, Claudia Ximena Ortiz, Bettarel, Yvan, Bouvier, Thierry, Auguet, Jean-Christophe
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Published Basel MDPI AG 11.08.2021
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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.
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.)
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Keywords coral reef fish
barcoding
enteric bacteriome
coral-macroalgal shift
microbial functions
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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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StartPage 1711
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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https://www.proquest.com/docview/2566031205
https://www.proquest.com/docview/2636742322
https://hal.science/hal-03357775
https://pubmed.ncbi.nlm.nih.gov/PMC8398123
https://doaj.org/article/73fad8da9e1345bbbdfe16e1d42b4997
Volume 9
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