Quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome

Abstract Background Upper gastrointestinal (GI) disorders and abdominal pain afflict between 12 and 30% of the worldwide population and research suggests these conditions are linked to the gut microbiome. Although large-intestine microbiota have been linked to several GI diseases, the microbiota of...

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Autores principales: Jacob T. Barlow, Gabriela Leite, Anna E. Romano, Rashin Sedighi, Christine Chang, Shreya Celly, Ali Rezaie, Ruchi Mathur, Mark Pimentel, Rustem F. Ismagilov
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Publicado: BMC 2021
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Acceso en línea:https://doaj.org/article/d7616074fe7d4cc19c4306f91566306b
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spelling oai:doaj.org-article:d7616074fe7d4cc19c4306f91566306b2021-11-07T12:12:28ZQuantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome10.1186/s40168-021-01162-22049-2618https://doaj.org/article/d7616074fe7d4cc19c4306f91566306b2021-11-01T00:00:00Zhttps://doi.org/10.1186/s40168-021-01162-2https://doaj.org/toc/2049-2618Abstract Background Upper gastrointestinal (GI) disorders and abdominal pain afflict between 12 and 30% of the worldwide population and research suggests these conditions are linked to the gut microbiome. Although large-intestine microbiota have been linked to several GI diseases, the microbiota of the human small intestine and its relation to human disease has been understudied. The small intestine is the major site for immune surveillance in the gut, and compared with the large intestine, it has greater than 100 times the surface area and a thinner and more permeable mucus layer. Results Using quantitative sequencing, we evaluated total and taxon-specific absolute microbial loads from 250 duodenal-aspirate samples and 21 paired duodenum-saliva samples from participants in the REIMAGINE study. Log-transformed total microbial loads spanned 5 logs and were normally distributed. Paired saliva-duodenum samples suggested potential transmission of oral microbes to the duodenum, including organisms from the HACEK group. Several taxa, including Klebsiella, Escherichia, Enterococcus, and Clostridium, seemed to displace strict anaerobes common in the duodenum, so we refer to these taxa as disruptors. Disruptor taxa were enriched in samples with high total microbial loads and in individuals with small intestinal bacterial overgrowth (SIBO). Absolute loads of disruptors were associated with more severe GI symptoms, highlighting the value of absolute taxon quantification when studying small-intestine health and function. Conclusion This study provides the largest dataset of the absolute abundance of microbiota from the human duodenum to date. The results reveal a clear relationship between the oral microbiota and the duodenal microbiota and suggest an association between the absolute abundance of disruptor taxa, SIBO, and the prevalence of severe GI symptoms. Video AbstractJacob T. BarlowGabriela LeiteAnna E. RomanoRashin SedighiChristine ChangShreya CellyAli RezaieRuchi MathurMark PimentelRustem F. IsmagilovBMCarticleDuodenumSalivaHACEKHuman small intestinal microbiomeIBSSIBOMicrobial ecologyQR100-130ENMicrobiome, Vol 9, Iss 1, Pp 1-17 (2021)
institution DOAJ
collection DOAJ
language EN
topic Duodenum
Saliva
HACEK
Human small intestinal microbiome
IBS
SIBO
Microbial ecology
QR100-130
spellingShingle Duodenum
Saliva
HACEK
Human small intestinal microbiome
IBS
SIBO
Microbial ecology
QR100-130
Jacob T. Barlow
Gabriela Leite
Anna E. Romano
Rashin Sedighi
Christine Chang
Shreya Celly
Ali Rezaie
Ruchi Mathur
Mark Pimentel
Rustem F. Ismagilov
Quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome
description Abstract Background Upper gastrointestinal (GI) disorders and abdominal pain afflict between 12 and 30% of the worldwide population and research suggests these conditions are linked to the gut microbiome. Although large-intestine microbiota have been linked to several GI diseases, the microbiota of the human small intestine and its relation to human disease has been understudied. The small intestine is the major site for immune surveillance in the gut, and compared with the large intestine, it has greater than 100 times the surface area and a thinner and more permeable mucus layer. Results Using quantitative sequencing, we evaluated total and taxon-specific absolute microbial loads from 250 duodenal-aspirate samples and 21 paired duodenum-saliva samples from participants in the REIMAGINE study. Log-transformed total microbial loads spanned 5 logs and were normally distributed. Paired saliva-duodenum samples suggested potential transmission of oral microbes to the duodenum, including organisms from the HACEK group. Several taxa, including Klebsiella, Escherichia, Enterococcus, and Clostridium, seemed to displace strict anaerobes common in the duodenum, so we refer to these taxa as disruptors. Disruptor taxa were enriched in samples with high total microbial loads and in individuals with small intestinal bacterial overgrowth (SIBO). Absolute loads of disruptors were associated with more severe GI symptoms, highlighting the value of absolute taxon quantification when studying small-intestine health and function. Conclusion This study provides the largest dataset of the absolute abundance of microbiota from the human duodenum to date. The results reveal a clear relationship between the oral microbiota and the duodenal microbiota and suggest an association between the absolute abundance of disruptor taxa, SIBO, and the prevalence of severe GI symptoms. Video Abstract
format article
author Jacob T. Barlow
Gabriela Leite
Anna E. Romano
Rashin Sedighi
Christine Chang
Shreya Celly
Ali Rezaie
Ruchi Mathur
Mark Pimentel
Rustem F. Ismagilov
author_facet Jacob T. Barlow
Gabriela Leite
Anna E. Romano
Rashin Sedighi
Christine Chang
Shreya Celly
Ali Rezaie
Ruchi Mathur
Mark Pimentel
Rustem F. Ismagilov
author_sort Jacob T. Barlow
title Quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome
title_short Quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome
title_full Quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome
title_fullStr Quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome
title_full_unstemmed Quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome
title_sort quantitative sequencing clarifies the role of disruptor taxa, oral microbiota, and strict anaerobes in the human small-intestine microbiome
publisher BMC
publishDate 2021
url https://doaj.org/article/d7616074fe7d4cc19c4306f91566306b
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