Qualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils

ABSTRACT Clinical interventions in the stomach have been linked to fecal microbiota alterations, suggesting a function of the stomach in gastrointestinal (GI) homeostasis. We sought to determine the taxonomic bacterial biogeography of the upper GI tract, including different sites within the human st...

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Autores principales: Philipp Wurm, Elisabeth Dörner, Christina Kremer, Julia Spranger, Cynthia Maddox, Bettina Halwachs, Ute Harrison, Thomas Blanchard, Rainer Haas, Christoph Högenauer, Gregor Gorkiewicz, W. Florian Fricke
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:13780553b34d4f50ad60611cd3ee73692021-12-02T18:39:46ZQualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils10.1128/mSystems.00262-182379-5077https://doaj.org/article/13780553b34d4f50ad60611cd3ee73692018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00262-18https://doaj.org/toc/2379-5077ABSTRACT Clinical interventions in the stomach have been linked to fecal microbiota alterations, suggesting a function of the stomach in gastrointestinal (GI) homeostasis. We sought to determine the taxonomic bacterial biogeography of the upper GI tract, including different sites within the human stomach (cardia, corpus, and antrum), adjacent upstream (esophagus) and downstream (duodenum) locations, and luminal contents (aspirate), as well as whole-stomach samples from mice and gerbils. Qualitative and quantitative DNA- and RNA-based taxonomic microbiota analyses were combined to study the relationship of relative and absolute bacterial abundances and transcriptionally active bacterial microbiota components in the stomach of humans and mice. Stomach microbiota compositions resembled those of esophagus and duodenum. However, along the descending GI tract, the relative abundances of specific oropharyngeal commensals decreased (Streptococcus) or increased (Rothia mucilaginosa, Porphyromonas, and Lachnospiraceae). Furthermore, the compositional similarity (weighted UniFrac) between stomach aspirates and esophageal biopsy samples increased with gastric Streptococcus relative abundance. In both human aspirate and mouse stomach samples, Firmicutes were more abundant among transcriptionally active bacteria than Bacteroidetes. The relative abundance of Firmicutes in the stomach was negatively correlated and that of Bacteroidetes was positively correlated with absolute bacterial abundance, suggesting a disproportionate increase of Bacteroidetes over Firmicutes at higher bacterial densities. Human, mouse, and gerbil stomach samples showed similarities at higher taxonomic levels but differences at lower taxonomic levels. Our findings suggest selective enrichment and depletion of specific bacterial taxa in the stomach and Firmicutes being transcriptionally more active than Bacteroidetes that increase in relative abundance with total bacterial load. IMPORTANCE Clinical stomach interventions, such as acid inhibition or bypass surgery, have been linked to fecal microbiota alterations. We demonstrate that the stomach microbiota largely overlaps those of adjacent gastrointestinal locations and identify gradual decreases and increases in the relative abundances of specific bacteria within the stomach, suggesting selective enrichment and depletion. Moreover, similarities between stomach and esophagus samples are proportional to the concentrations of Streptococcus (Firmicutes) in the stomach. The relative abundance of Firmicutes in the stomach, compared to that of Bacteroidetes, is increased in RNA relative to DNA, indicating higher transcriptional activity. Moreover, increased absolute bacterial loads are associated with decreased relative abundance of Firmicutes and higher relative abundance of Bacteroidetes. Our findings characterize the stomach microbiota as influenced by Bacteroidetes influx against a background of transcriptionally more active Firmicutes. Human, mouse, and gerbil stomach microbiotas differ at lower taxonomic levels, which might affect the utility of these model organisms.Philipp WurmElisabeth DörnerChristina KremerJulia SprangerCynthia MaddoxBettina HalwachsUte HarrisonThomas BlanchardRainer HaasChristoph HögenauerGregor GorkiewiczW. Florian FrickeAmerican Society for Microbiologyarticle16S rRNAabsolute abundancequantitative microbiota analysisstomach microbiotatranscriptional activityMicrobiologyQR1-502ENmSystems, Vol 3, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic 16S rRNA
absolute abundance
quantitative microbiota analysis
stomach microbiota
transcriptional activity
Microbiology
QR1-502
spellingShingle 16S rRNA
absolute abundance
quantitative microbiota analysis
stomach microbiota
transcriptional activity
Microbiology
QR1-502
Philipp Wurm
Elisabeth Dörner
Christina Kremer
Julia Spranger
Cynthia Maddox
Bettina Halwachs
Ute Harrison
Thomas Blanchard
Rainer Haas
Christoph Högenauer
Gregor Gorkiewicz
W. Florian Fricke
Qualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils
description ABSTRACT Clinical interventions in the stomach have been linked to fecal microbiota alterations, suggesting a function of the stomach in gastrointestinal (GI) homeostasis. We sought to determine the taxonomic bacterial biogeography of the upper GI tract, including different sites within the human stomach (cardia, corpus, and antrum), adjacent upstream (esophagus) and downstream (duodenum) locations, and luminal contents (aspirate), as well as whole-stomach samples from mice and gerbils. Qualitative and quantitative DNA- and RNA-based taxonomic microbiota analyses were combined to study the relationship of relative and absolute bacterial abundances and transcriptionally active bacterial microbiota components in the stomach of humans and mice. Stomach microbiota compositions resembled those of esophagus and duodenum. However, along the descending GI tract, the relative abundances of specific oropharyngeal commensals decreased (Streptococcus) or increased (Rothia mucilaginosa, Porphyromonas, and Lachnospiraceae). Furthermore, the compositional similarity (weighted UniFrac) between stomach aspirates and esophageal biopsy samples increased with gastric Streptococcus relative abundance. In both human aspirate and mouse stomach samples, Firmicutes were more abundant among transcriptionally active bacteria than Bacteroidetes. The relative abundance of Firmicutes in the stomach was negatively correlated and that of Bacteroidetes was positively correlated with absolute bacterial abundance, suggesting a disproportionate increase of Bacteroidetes over Firmicutes at higher bacterial densities. Human, mouse, and gerbil stomach samples showed similarities at higher taxonomic levels but differences at lower taxonomic levels. Our findings suggest selective enrichment and depletion of specific bacterial taxa in the stomach and Firmicutes being transcriptionally more active than Bacteroidetes that increase in relative abundance with total bacterial load. IMPORTANCE Clinical stomach interventions, such as acid inhibition or bypass surgery, have been linked to fecal microbiota alterations. We demonstrate that the stomach microbiota largely overlaps those of adjacent gastrointestinal locations and identify gradual decreases and increases in the relative abundances of specific bacteria within the stomach, suggesting selective enrichment and depletion. Moreover, similarities between stomach and esophagus samples are proportional to the concentrations of Streptococcus (Firmicutes) in the stomach. The relative abundance of Firmicutes in the stomach, compared to that of Bacteroidetes, is increased in RNA relative to DNA, indicating higher transcriptional activity. Moreover, increased absolute bacterial loads are associated with decreased relative abundance of Firmicutes and higher relative abundance of Bacteroidetes. Our findings characterize the stomach microbiota as influenced by Bacteroidetes influx against a background of transcriptionally more active Firmicutes. Human, mouse, and gerbil stomach microbiotas differ at lower taxonomic levels, which might affect the utility of these model organisms.
format article
author Philipp Wurm
Elisabeth Dörner
Christina Kremer
Julia Spranger
Cynthia Maddox
Bettina Halwachs
Ute Harrison
Thomas Blanchard
Rainer Haas
Christoph Högenauer
Gregor Gorkiewicz
W. Florian Fricke
author_facet Philipp Wurm
Elisabeth Dörner
Christina Kremer
Julia Spranger
Cynthia Maddox
Bettina Halwachs
Ute Harrison
Thomas Blanchard
Rainer Haas
Christoph Högenauer
Gregor Gorkiewicz
W. Florian Fricke
author_sort Philipp Wurm
title Qualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils
title_short Qualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils
title_full Qualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils
title_fullStr Qualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils
title_full_unstemmed Qualitative and Quantitative DNA- and RNA-Based Analysis of the Bacterial Stomach Microbiota in Humans, Mice, and Gerbils
title_sort qualitative and quantitative dna- and rna-based analysis of the bacterial stomach microbiota in humans, mice, and gerbils
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/13780553b34d4f50ad60611cd3ee7369
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