Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans

ABSTRACT Although the microbiota in the proximal gastrointestinal (GI) tract have been implicated in health and disease, much about these microbes remains understudied compared to those in the distal GI tract. This study characterized the microbiota across multiple proximal GI sites over time in hea...

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Autores principales:	Anna M. Seekatz, Matthew K. Schnizlein, Mark J. Koenigsknecht, Jason R. Baker, William L. Hasler, Barry E. Bleske, Vincent B. Young, Duxin Sun
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	mesalamine microbiota pH small intestine stomach Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2f67e783b33d423f9c091ecddb7ca29e
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spelling	oai:doaj.org-article:2f67e783b33d423f9c091ecddb7ca29e2021-11-15T15:22:22ZSpatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans10.1128/mSphere.00126-192379-5042https://doaj.org/article/2f67e783b33d423f9c091ecddb7ca29e2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00126-19https://doaj.org/toc/2379-5042ABSTRACT Although the microbiota in the proximal gastrointestinal (GI) tract have been implicated in health and disease, much about these microbes remains understudied compared to those in the distal GI tract. This study characterized the microbiota across multiple proximal GI sites over time in healthy individuals. As part of a study of the pharmacokinetics of oral mesalamine administration, healthy, fasted volunteers (n = 8; 10 observation periods total) were orally intubated with a four-lumen catheter with multiple aspiration ports. Samples were taken from stomach, duodenal, and multiple jejunal sites, sampling hourly (≤7 h) to measure mesalamine (administered at t = 0), pH, and 16S rRNA gene-based composition. We observed a predominance of Firmicutes across proximal GI sites, with significant variation compared to stool. The microbiota was more similar within individuals over time than between subjects, with the fecal microbiota being unique from that of the small intestine. The stomach and duodenal microbiota displayed highest intraindividual variability compared to jejunal sites, which were more stable across time. We observed significant correlations in the duodenal microbial composition with changes in pH; linear mixed models identified positive correlations with multiple Streptococcus operational taxonomic units (OTUs) and negative correlations with multiple Prevotella and Pasteurellaceae OTUs. Few OTUs correlated with mesalamine concentration. The stomach and duodenal microbiota exhibited greater compositional dynamics than the jejunum. Short-term fluctuations in the duodenal microbiota were correlated with pH. Given the unique characteristics and dynamics of the proximal GI tract microbiota, it is important to consider these local environments in health and disease states. IMPORTANCE The gut microbiota are linked to a variety of gastrointestinal diseases, including inflammatory bowel disease. Despite this importance, microbiota dynamics in the upper gastrointestinal tract are understudied. Our article seeks to understand what factors impact microbiota dynamics in the healthy human upper gut. We found that the upper gastrointestinal tract contains consistently prevalent bacterial OTUs that dominate the overall community. Microbiota variability is highest in the stomach and duodenum and correlates with pH.Anna M. SeekatzMatthew K. SchnizleinMark J. KoenigsknechtJason R. BakerWilliam L. HaslerBarry E. BleskeVincent B. YoungDuxin SunAmerican Society for MicrobiologyarticlemesalaminemicrobiotapHsmall intestinestomachMicrobiologyQR1-502ENmSphere, Vol 4, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	mesalamine microbiota pH small intestine stomach Microbiology QR1-502
spellingShingle	mesalamine microbiota pH small intestine stomach Microbiology QR1-502 Anna M. Seekatz Matthew K. Schnizlein Mark J. Koenigsknecht Jason R. Baker William L. Hasler Barry E. Bleske Vincent B. Young Duxin Sun Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans
description	ABSTRACT Although the microbiota in the proximal gastrointestinal (GI) tract have been implicated in health and disease, much about these microbes remains understudied compared to those in the distal GI tract. This study characterized the microbiota across multiple proximal GI sites over time in healthy individuals. As part of a study of the pharmacokinetics of oral mesalamine administration, healthy, fasted volunteers (n = 8; 10 observation periods total) were orally intubated with a four-lumen catheter with multiple aspiration ports. Samples were taken from stomach, duodenal, and multiple jejunal sites, sampling hourly (≤7 h) to measure mesalamine (administered at t = 0), pH, and 16S rRNA gene-based composition. We observed a predominance of Firmicutes across proximal GI sites, with significant variation compared to stool. The microbiota was more similar within individuals over time than between subjects, with the fecal microbiota being unique from that of the small intestine. The stomach and duodenal microbiota displayed highest intraindividual variability compared to jejunal sites, which were more stable across time. We observed significant correlations in the duodenal microbial composition with changes in pH; linear mixed models identified positive correlations with multiple Streptococcus operational taxonomic units (OTUs) and negative correlations with multiple Prevotella and Pasteurellaceae OTUs. Few OTUs correlated with mesalamine concentration. The stomach and duodenal microbiota exhibited greater compositional dynamics than the jejunum. Short-term fluctuations in the duodenal microbiota were correlated with pH. Given the unique characteristics and dynamics of the proximal GI tract microbiota, it is important to consider these local environments in health and disease states. IMPORTANCE The gut microbiota are linked to a variety of gastrointestinal diseases, including inflammatory bowel disease. Despite this importance, microbiota dynamics in the upper gastrointestinal tract are understudied. Our article seeks to understand what factors impact microbiota dynamics in the healthy human upper gut. We found that the upper gastrointestinal tract contains consistently prevalent bacterial OTUs that dominate the overall community. Microbiota variability is highest in the stomach and duodenum and correlates with pH.
format	article
author	Anna M. Seekatz Matthew K. Schnizlein Mark J. Koenigsknecht Jason R. Baker William L. Hasler Barry E. Bleske Vincent B. Young Duxin Sun
author_facet	Anna M. Seekatz Matthew K. Schnizlein Mark J. Koenigsknecht Jason R. Baker William L. Hasler Barry E. Bleske Vincent B. Young Duxin Sun
author_sort	Anna M. Seekatz
title	Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans
title_short	Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans
title_full	Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans
title_fullStr	Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans
title_full_unstemmed	Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans
title_sort	spatial and temporal analysis of the stomach and small-intestinal microbiota in fasted healthy humans
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/2f67e783b33d423f9c091ecddb7ca29e
work_keys_str_mv	AT annamseekatz spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans AT matthewkschnizlein spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans AT markjkoenigsknecht spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans AT jasonrbaker spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans AT williamlhasler spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans AT barryebleske spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans AT vincentbyoung spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans AT duxinsun spatialandtemporalanalysisofthestomachandsmallintestinalmicrobiotainfastedhealthyhumans
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Spatial and Temporal Analysis of the Stomach and Small-Intestinal Microbiota in Fasted Healthy Humans

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