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Early-life gut dysbiosis linked to juvenile mortality in ostriches

BACKGROUND: Imbalances in the gut microbial community (dysbiosis) of vertebrates have been associated with several gastrointestinal and autoimmune diseases. However, it is unclear which taxa are associated with gut dysbiosis, and if particular gut regions or specific time periods during ontogeny are...

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Autores principales: Videvall, Elin, Song, Se Jin, Bensch, Hanna M., Strandh, Maria, Engelbrecht, Anel, Serfontein, Naomi, Hellgren, Olof, Olivier, Adriaan, Cloete, Schalk, Knight, Rob, Cornwallis, Charlie K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7552511/
https://www.ncbi.nlm.nih.gov/pubmed/33046114
http://dx.doi.org/10.1186/s40168-020-00925-7
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author Videvall, Elin
Song, Se Jin
Bensch, Hanna M.
Strandh, Maria
Engelbrecht, Anel
Serfontein, Naomi
Hellgren, Olof
Olivier, Adriaan
Cloete, Schalk
Knight, Rob
Cornwallis, Charlie K.
author_facet Videvall, Elin
Song, Se Jin
Bensch, Hanna M.
Strandh, Maria
Engelbrecht, Anel
Serfontein, Naomi
Hellgren, Olof
Olivier, Adriaan
Cloete, Schalk
Knight, Rob
Cornwallis, Charlie K.
author_sort Videvall, Elin
collection PubMed
description BACKGROUND: Imbalances in the gut microbial community (dysbiosis) of vertebrates have been associated with several gastrointestinal and autoimmune diseases. However, it is unclear which taxa are associated with gut dysbiosis, and if particular gut regions or specific time periods during ontogeny are more susceptible. We also know very little of this process in non-model organisms, despite an increasing realization of the general importance of gut microbiota for health. METHODS: Here, we examine the changes that occur in the microbiome during dysbiosis in different parts of the gastrointestinal tract in a long-lived bird with high juvenile mortality, the ostrich (Struthio camelus). We evaluated the 16S rRNA gene composition of the ileum, cecum, and colon of 68 individuals that died of suspected enterocolitis during the first 3 months of life (diseased individuals), and of 50 healthy individuals that were euthanized as age-matched controls. We combined these data with longitudinal environmental and fecal sampling to identify potential sources of pathogenic bacteria and to unravel at which stage of development dysbiosis-associated bacteria emerge. RESULTS: Diseased individuals had drastically lower microbial alpha diversity and differed substantially in their microbial beta diversity from control individuals in all three regions of the gastrointestinal tract. The clear relationship between low diversity and disease was consistent across all ages in the ileum, but decreased with age in the cecum and colon. Several taxa were associated with mortality (Enterobacteriaceae, Peptostreptococcaceae, Porphyromonadaceae, Clostridium), while others were associated with health (Lachnospiraceae, Ruminococcaceae, Erysipelotrichaceae, Turicibacter, Roseburia). Environmental samples showed no evidence of dysbiosis-associated bacteria being present in either the food, water, or soil substrate. Instead, the repeated fecal sampling showed that pathobionts were already present shortly after hatching and proliferated in individuals with low microbial diversity, resulting in high mortality several weeks later. CONCLUSIONS: Identifying the origins of pathobionts in neonates and the factors that subsequently influence the establishment of diverse gut microbiota may be key to understanding dysbiosis and host development.
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spelling pubmed-75525112020-10-13 Early-life gut dysbiosis linked to juvenile mortality in ostriches Videvall, Elin Song, Se Jin Bensch, Hanna M. Strandh, Maria Engelbrecht, Anel Serfontein, Naomi Hellgren, Olof Olivier, Adriaan Cloete, Schalk Knight, Rob Cornwallis, Charlie K. Microbiome Research BACKGROUND: Imbalances in the gut microbial community (dysbiosis) of vertebrates have been associated with several gastrointestinal and autoimmune diseases. However, it is unclear which taxa are associated with gut dysbiosis, and if particular gut regions or specific time periods during ontogeny are more susceptible. We also know very little of this process in non-model organisms, despite an increasing realization of the general importance of gut microbiota for health. METHODS: Here, we examine the changes that occur in the microbiome during dysbiosis in different parts of the gastrointestinal tract in a long-lived bird with high juvenile mortality, the ostrich (Struthio camelus). We evaluated the 16S rRNA gene composition of the ileum, cecum, and colon of 68 individuals that died of suspected enterocolitis during the first 3 months of life (diseased individuals), and of 50 healthy individuals that were euthanized as age-matched controls. We combined these data with longitudinal environmental and fecal sampling to identify potential sources of pathogenic bacteria and to unravel at which stage of development dysbiosis-associated bacteria emerge. RESULTS: Diseased individuals had drastically lower microbial alpha diversity and differed substantially in their microbial beta diversity from control individuals in all three regions of the gastrointestinal tract. The clear relationship between low diversity and disease was consistent across all ages in the ileum, but decreased with age in the cecum and colon. Several taxa were associated with mortality (Enterobacteriaceae, Peptostreptococcaceae, Porphyromonadaceae, Clostridium), while others were associated with health (Lachnospiraceae, Ruminococcaceae, Erysipelotrichaceae, Turicibacter, Roseburia). Environmental samples showed no evidence of dysbiosis-associated bacteria being present in either the food, water, or soil substrate. Instead, the repeated fecal sampling showed that pathobionts were already present shortly after hatching and proliferated in individuals with low microbial diversity, resulting in high mortality several weeks later. CONCLUSIONS: Identifying the origins of pathobionts in neonates and the factors that subsequently influence the establishment of diverse gut microbiota may be key to understanding dysbiosis and host development. BioMed Central 2020-10-12 /pmc/articles/PMC7552511/ /pubmed/33046114 http://dx.doi.org/10.1186/s40168-020-00925-7 Text en © The Author(s) 2020 Open AccessThis 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/. The Creative Commons Public Domain Dedication waiver (http://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
Videvall, Elin
Song, Se Jin
Bensch, Hanna M.
Strandh, Maria
Engelbrecht, Anel
Serfontein, Naomi
Hellgren, Olof
Olivier, Adriaan
Cloete, Schalk
Knight, Rob
Cornwallis, Charlie K.
Early-life gut dysbiosis linked to juvenile mortality in ostriches
title Early-life gut dysbiosis linked to juvenile mortality in ostriches
title_full Early-life gut dysbiosis linked to juvenile mortality in ostriches
title_fullStr Early-life gut dysbiosis linked to juvenile mortality in ostriches
title_full_unstemmed Early-life gut dysbiosis linked to juvenile mortality in ostriches
title_short Early-life gut dysbiosis linked to juvenile mortality in ostriches
title_sort early-life gut dysbiosis linked to juvenile mortality in ostriches
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7552511/
https://www.ncbi.nlm.nih.gov/pubmed/33046114
http://dx.doi.org/10.1186/s40168-020-00925-7
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