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Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus

BACKGROUND: Gut microbiota play a key role in the nutrition of many marine herbivorous fishes through hindgut fermentation of seaweed. Gut microbiota composition in the herbivorous fish Kyphosus sydneyanus (family Kyphosidae) varies between individuals and gut sections, raising two questions: (i) is...

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Autores principales: Pisaniello, Alessandro, Handley, Kim M., White, W. Lindsey, Angert, Esther R., Boey, Jian Sheng, Clements, Kendall D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10540440/
https://www.ncbi.nlm.nih.gov/pubmed/37773099
http://dx.doi.org/10.1186/s12866-023-03025-2
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author Pisaniello, Alessandro
Handley, Kim M.
White, W. Lindsey
Angert, Esther R.
Boey, Jian Sheng
Clements, Kendall D.
author_facet Pisaniello, Alessandro
Handley, Kim M.
White, W. Lindsey
Angert, Esther R.
Boey, Jian Sheng
Clements, Kendall D.
author_sort Pisaniello, Alessandro
collection PubMed
description BACKGROUND: Gut microbiota play a key role in the nutrition of many marine herbivorous fishes through hindgut fermentation of seaweed. Gut microbiota composition in the herbivorous fish Kyphosus sydneyanus (family Kyphosidae) varies between individuals and gut sections, raising two questions: (i) is community composition stable over time, especially given seasonal shifts in storage metabolites of dietary brown algae, and (ii) what processes influence community assembly in the hindgut? RESULTS: We examined variation in community composition in gut lumen and mucosa samples from three hindgut sections of K. sydneyanus collected at various time points in 2020 and 2021 from reefs near Great Barrier Island, New Zealand. 16S rRNA gene analysis was used to characterize microbial community composition, diversity and estimated density. Differences in community composition between gut sections remained relatively stable over time, with little evidence of temporal variation. Clostridia dominated the proximal hindgut sections and Bacteroidia the most distal section. Differences were detected in microbial composition between lumen and mucosa, especially at genus level. CONCLUSIONS: High variation in community composition and estimated bacterial density among individual fish combined with low variation in community composition temporally suggests that initial community assembly involved environmental selection and random sampling/neutral effects. Community stability following colonisation could also be influenced by historical contingency, where early colonizing members of the community may have a selective advantage. The impact of temporal changes in the algae may be limited by the dynamics of substrate depletion along the gut following feeding, i.e. the depletion of storage metabolites in the proximal hindgut. Estimated bacterial density, showed that Bacteroidota has the highest density (copies/mL) in distal-most lumen section V, where SCFA concentrations are highest. Bacteroidota genera Alistipes and Rikenella may play important roles in the breakdown of seaweed into useful compounds for the fish host. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-03025-2.
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spelling pubmed-105404402023-09-30 Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus Pisaniello, Alessandro Handley, Kim M. White, W. Lindsey Angert, Esther R. Boey, Jian Sheng Clements, Kendall D. BMC Microbiol Research BACKGROUND: Gut microbiota play a key role in the nutrition of many marine herbivorous fishes through hindgut fermentation of seaweed. Gut microbiota composition in the herbivorous fish Kyphosus sydneyanus (family Kyphosidae) varies between individuals and gut sections, raising two questions: (i) is community composition stable over time, especially given seasonal shifts in storage metabolites of dietary brown algae, and (ii) what processes influence community assembly in the hindgut? RESULTS: We examined variation in community composition in gut lumen and mucosa samples from three hindgut sections of K. sydneyanus collected at various time points in 2020 and 2021 from reefs near Great Barrier Island, New Zealand. 16S rRNA gene analysis was used to characterize microbial community composition, diversity and estimated density. Differences in community composition between gut sections remained relatively stable over time, with little evidence of temporal variation. Clostridia dominated the proximal hindgut sections and Bacteroidia the most distal section. Differences were detected in microbial composition between lumen and mucosa, especially at genus level. CONCLUSIONS: High variation in community composition and estimated bacterial density among individual fish combined with low variation in community composition temporally suggests that initial community assembly involved environmental selection and random sampling/neutral effects. Community stability following colonisation could also be influenced by historical contingency, where early colonizing members of the community may have a selective advantage. The impact of temporal changes in the algae may be limited by the dynamics of substrate depletion along the gut following feeding, i.e. the depletion of storage metabolites in the proximal hindgut. Estimated bacterial density, showed that Bacteroidota has the highest density (copies/mL) in distal-most lumen section V, where SCFA concentrations are highest. Bacteroidota genera Alistipes and Rikenella may play important roles in the breakdown of seaweed into useful compounds for the fish host. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-03025-2. BioMed Central 2023-09-29 /pmc/articles/PMC10540440/ /pubmed/37773099 http://dx.doi.org/10.1186/s12866-023-03025-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Pisaniello, Alessandro
Handley, Kim M.
White, W. Lindsey
Angert, Esther R.
Boey, Jian Sheng
Clements, Kendall D.
Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus
title Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus
title_full Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus
title_fullStr Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus
title_full_unstemmed Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus
title_short Host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish Kyphosus sydneyanus
title_sort host individual and gut location are more important in gut microbiota community composition than temporal variation in the marine herbivorous fish kyphosus sydneyanus
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10540440/
https://www.ncbi.nlm.nih.gov/pubmed/37773099
http://dx.doi.org/10.1186/s12866-023-03025-2
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