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Early-life gut dysbiosis linked to juvenile mortality in ostriches

Videvall, Elin LU ; Song, Se Jin ; Bensch, Hanna M. ; Strandh, Maria LU ; Engelbrecht, Anel ; Serfontein, Naomi ; Hellgren, Olof LU ; Olivier, Adriaan ; Cloete, Schalk and Knight, Rob , et al. (2020) In Microbiome 8(1).
Abstract

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,... (More)

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. [MediaObject not available: See fulltext.]

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Disease, Dysbacteriosis, Gastrointestinal tract, Gut microbiota, Inflammation, Microbial diversity
in
Microbiome
volume
8
issue
1
article number
147
publisher
BioMed Central (BMC)
external identifiers
  • pmid:33046114
  • scopus:85092599033
ISSN
2049-2618
DOI
10.1186/s40168-020-00925-7
language
English
LU publication?
yes
id
974dfb78-7a89-40f0-9a10-c53c5b1bf508
date added to LUP
2020-11-06 10:34:25
date last changed
2024-03-05 12:25:18
@article{974dfb78-7a89-40f0-9a10-c53c5b1bf508,
  abstract     = {{<p>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. [MediaObject not available: See fulltext.] </p>}},
  author       = {{Videvall, Elin and Song, Se Jin and Bensch, Hanna M. and Strandh, Maria and Engelbrecht, Anel and Serfontein, Naomi and Hellgren, Olof and Olivier, Adriaan and Cloete, Schalk and Knight, Rob and Cornwallis, Charlie K.}},
  issn         = {{2049-2618}},
  keywords     = {{Disease; Dysbacteriosis; Gastrointestinal tract; Gut microbiota; Inflammation; Microbial diversity}},
  language     = {{eng}},
  number       = {{1}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{Microbiome}},
  title        = {{Early-life gut dysbiosis linked to juvenile mortality in ostriches}},
  url          = {{http://dx.doi.org/10.1186/s40168-020-00925-7}},
  doi          = {{10.1186/s40168-020-00925-7}},
  volume       = {{8}},
  year         = {{2020}},
}