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Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish

Many marine herbivorous fishes harbour diverse microbial communities in the hindgut that can play important roles in host health and nutrition. Kyphosus sydneyanus is a temperate marine herbivorous fish that feeds predominantly on brown seaweeds. We employed 16S rRNA gene amplicon sequencing and gas...

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Autores principales: Pardesi, Bikiran, Roberton, Anthony M., Lee, Kevin C., Angert, Esther R., Rosendale, Douglas I., Boycheva, Svetlana, White, William L., Clements, Kendall D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306998/
https://www.ncbi.nlm.nih.gov/pubmed/35152505
http://dx.doi.org/10.1111/mec.16394
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author Pardesi, Bikiran
Roberton, Anthony M.
Lee, Kevin C.
Angert, Esther R.
Rosendale, Douglas I.
Boycheva, Svetlana
White, William L.
Clements, Kendall D.
author_facet Pardesi, Bikiran
Roberton, Anthony M.
Lee, Kevin C.
Angert, Esther R.
Rosendale, Douglas I.
Boycheva, Svetlana
White, William L.
Clements, Kendall D.
author_sort Pardesi, Bikiran
collection PubMed
description Many marine herbivorous fishes harbour diverse microbial communities in the hindgut that can play important roles in host health and nutrition. Kyphosus sydneyanus is a temperate marine herbivorous fish that feeds predominantly on brown seaweeds. We employed 16S rRNA gene amplicon sequencing and gas chromatography to characterize microbial communities and their metabolites in different hindgut regions of six K. sydneyanus. Measurements were confined to three distal sections of the intestine, labelled III, IV and V from anterior to posterior. A total of 625 operational taxonomic units from 20 phyla and 123 genera were obtained. Bacteroidota, Firmicutes and Proteobacteria were the major phyla in mean relative abundance, which varied along the gut. Firmicutes (76%) was the most dominant group in section III, whereas Bacteroidota (69.3%) dominated section V. Total short‐chain fatty acid (SCFA) concentration was highest in sections IV and V, confirming active fermentation in these two most distal sections. The abundance of Bacteroidota correlated with propionate concentration in section V, while Firmicutes positively correlated with formate in sections III and IV. Acetate levels were highest in sections IV and V, which correlated with abundance of Bacteroidota. Despite differences in gut microbial community composition, SCFA profiles were consistent between individual fish in the different hindgut regions of K. sydneyanus, although proportions of SCFAs differed among gut sections. These findings demonstrate functional compartmentalization of the hindgut microbial community, highlighting the need for regional sampling when interpreting overall microbiome function. These results support previous work suggesting that hindgut microbiota in marine herbivorous fish are important to nutrition in some host species by converting dietary carbohydrates into metabolically useful SCFAs.
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spelling pubmed-93069982022-07-28 Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish Pardesi, Bikiran Roberton, Anthony M. Lee, Kevin C. Angert, Esther R. Rosendale, Douglas I. Boycheva, Svetlana White, William L. Clements, Kendall D. Mol Ecol ORIGINAL ARTICLES Many marine herbivorous fishes harbour diverse microbial communities in the hindgut that can play important roles in host health and nutrition. Kyphosus sydneyanus is a temperate marine herbivorous fish that feeds predominantly on brown seaweeds. We employed 16S rRNA gene amplicon sequencing and gas chromatography to characterize microbial communities and their metabolites in different hindgut regions of six K. sydneyanus. Measurements were confined to three distal sections of the intestine, labelled III, IV and V from anterior to posterior. A total of 625 operational taxonomic units from 20 phyla and 123 genera were obtained. Bacteroidota, Firmicutes and Proteobacteria were the major phyla in mean relative abundance, which varied along the gut. Firmicutes (76%) was the most dominant group in section III, whereas Bacteroidota (69.3%) dominated section V. Total short‐chain fatty acid (SCFA) concentration was highest in sections IV and V, confirming active fermentation in these two most distal sections. The abundance of Bacteroidota correlated with propionate concentration in section V, while Firmicutes positively correlated with formate in sections III and IV. Acetate levels were highest in sections IV and V, which correlated with abundance of Bacteroidota. Despite differences in gut microbial community composition, SCFA profiles were consistent between individual fish in the different hindgut regions of K. sydneyanus, although proportions of SCFAs differed among gut sections. These findings demonstrate functional compartmentalization of the hindgut microbial community, highlighting the need for regional sampling when interpreting overall microbiome function. These results support previous work suggesting that hindgut microbiota in marine herbivorous fish are important to nutrition in some host species by converting dietary carbohydrates into metabolically useful SCFAs. John Wiley and Sons Inc. 2022-02-21 2022-04 /pmc/articles/PMC9306998/ /pubmed/35152505 http://dx.doi.org/10.1111/mec.16394 Text en © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle ORIGINAL ARTICLES
Pardesi, Bikiran
Roberton, Anthony M.
Lee, Kevin C.
Angert, Esther R.
Rosendale, Douglas I.
Boycheva, Svetlana
White, William L.
Clements, Kendall D.
Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish
title Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish
title_full Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish
title_fullStr Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish
title_full_unstemmed Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish
title_short Distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish
title_sort distinct microbiota composition and fermentation products indicate functional compartmentalization in the hindgut of a marine herbivorous fish
topic ORIGINAL ARTICLES
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9306998/
https://www.ncbi.nlm.nih.gov/pubmed/35152505
http://dx.doi.org/10.1111/mec.16394
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