Cargando…

The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon

BACKGROUND: The upper half of the human small intestine, known as the jejunum, is the primary site for absorption of nutrient-derived carbohydrates, amino acids, small peptides, and vitamins. In contrast to the colon, which contains 10(11)–10(12) colony forming units of bacteria per ml (CFU/ml), the...

Descripción completa

Detalles Bibliográficos
Autores principales: Sundin, Olof H., Mendoza-Ladd, Antonio, Zeng, Mingtao, Diaz-Arévalo, Diana, Morales, Elisa, Fagan, B. Matthew, Ordoñez, Javier, Velez, Philip, Antony, Nishaal, McCallum, Richard W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513040/
https://www.ncbi.nlm.nih.gov/pubmed/28716079
http://dx.doi.org/10.1186/s12866-017-1059-6
_version_ 1783250582483501056
author Sundin, Olof H.
Mendoza-Ladd, Antonio
Zeng, Mingtao
Diaz-Arévalo, Diana
Morales, Elisa
Fagan, B. Matthew
Ordoñez, Javier
Velez, Philip
Antony, Nishaal
McCallum, Richard W.
author_facet Sundin, Olof H.
Mendoza-Ladd, Antonio
Zeng, Mingtao
Diaz-Arévalo, Diana
Morales, Elisa
Fagan, B. Matthew
Ordoñez, Javier
Velez, Philip
Antony, Nishaal
McCallum, Richard W.
author_sort Sundin, Olof H.
collection PubMed
description BACKGROUND: The upper half of the human small intestine, known as the jejunum, is the primary site for absorption of nutrient-derived carbohydrates, amino acids, small peptides, and vitamins. In contrast to the colon, which contains 10(11)–10(12) colony forming units of bacteria per ml (CFU/ml), the normal jejunum generally ranges from 10(3) to 10(5) CFU per ml. Because invasive procedures are required to access the jejunum, much less is known about its bacterial microbiota. Bacteria inhabiting the jejunal lumen have been investigated by classical culture techniques, but not by culture-independent metagenomics. RESULTS: The lumen of the upper jejunum was sampled during enteroscopy of 20 research subjects. Culture on aerobic and anaerobic media gave live bacterial counts ranging from 5.8 × 10(3) CFU/ml to 8.0 × 10(6) CFU/ml. DNA from the same samples was analyzed by 16S rRNA gene-specific quantitative PCR, yielding values from 1.5 × 10(5) to 3.1 × 10(7) bacterial genomes per ml. When calculated for each sample, estimated bacterial viability ranged from effectively 100% to a low of 0.3%. 16S rRNA metagenomic analysis of uncultured bacteria by Illumina MiSeq sequencing gave detailed microbial composition by phylum, genus and species. The genera Streptococcus, Prevotella, Veillonella and Fusobacterium, were especially abundant, as well as non-oral genera including Escherichia, Klebsiella, and Citrobacter. The jejunum was devoid of the genera Alistipes, Ruminococcus, Faecalibacterium, and other extreme anaerobes abundant in the colon. In patients with higher bacterial loads, there was no significant change in microbial species composition. CONCLUSIONS: The jejunal lumen contains a distinctive bacterial population consisting primarily of facultative anaerobes and oxygen-tolerant obligate anaerobes similar to those found in the oral cavity. However, the frequent abundance of Enterobacteriaceae represents a major difference from oral microbiota. Although a few genera are shared with the colon, we found no evidence for retrograde movement of the most abundant colonic microbes to the jejunum. Some individuals had much higher bacterial loads, but this was not correlated with decreases in bacterial species diversity or other evidence of dysbiosis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-017-1059-6) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5513040
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-55130402017-07-19 The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon Sundin, Olof H. Mendoza-Ladd, Antonio Zeng, Mingtao Diaz-Arévalo, Diana Morales, Elisa Fagan, B. Matthew Ordoñez, Javier Velez, Philip Antony, Nishaal McCallum, Richard W. BMC Microbiol Research Article BACKGROUND: The upper half of the human small intestine, known as the jejunum, is the primary site for absorption of nutrient-derived carbohydrates, amino acids, small peptides, and vitamins. In contrast to the colon, which contains 10(11)–10(12) colony forming units of bacteria per ml (CFU/ml), the normal jejunum generally ranges from 10(3) to 10(5) CFU per ml. Because invasive procedures are required to access the jejunum, much less is known about its bacterial microbiota. Bacteria inhabiting the jejunal lumen have been investigated by classical culture techniques, but not by culture-independent metagenomics. RESULTS: The lumen of the upper jejunum was sampled during enteroscopy of 20 research subjects. Culture on aerobic and anaerobic media gave live bacterial counts ranging from 5.8 × 10(3) CFU/ml to 8.0 × 10(6) CFU/ml. DNA from the same samples was analyzed by 16S rRNA gene-specific quantitative PCR, yielding values from 1.5 × 10(5) to 3.1 × 10(7) bacterial genomes per ml. When calculated for each sample, estimated bacterial viability ranged from effectively 100% to a low of 0.3%. 16S rRNA metagenomic analysis of uncultured bacteria by Illumina MiSeq sequencing gave detailed microbial composition by phylum, genus and species. The genera Streptococcus, Prevotella, Veillonella and Fusobacterium, were especially abundant, as well as non-oral genera including Escherichia, Klebsiella, and Citrobacter. The jejunum was devoid of the genera Alistipes, Ruminococcus, Faecalibacterium, and other extreme anaerobes abundant in the colon. In patients with higher bacterial loads, there was no significant change in microbial species composition. CONCLUSIONS: The jejunal lumen contains a distinctive bacterial population consisting primarily of facultative anaerobes and oxygen-tolerant obligate anaerobes similar to those found in the oral cavity. However, the frequent abundance of Enterobacteriaceae represents a major difference from oral microbiota. Although a few genera are shared with the colon, we found no evidence for retrograde movement of the most abundant colonic microbes to the jejunum. Some individuals had much higher bacterial loads, but this was not correlated with decreases in bacterial species diversity or other evidence of dysbiosis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-017-1059-6) contains supplementary material, which is available to authorized users. BioMed Central 2017-07-17 /pmc/articles/PMC5513040/ /pubmed/28716079 http://dx.doi.org/10.1186/s12866-017-1059-6 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research Article
Sundin, Olof H.
Mendoza-Ladd, Antonio
Zeng, Mingtao
Diaz-Arévalo, Diana
Morales, Elisa
Fagan, B. Matthew
Ordoñez, Javier
Velez, Philip
Antony, Nishaal
McCallum, Richard W.
The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon
title The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon
title_full The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon
title_fullStr The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon
title_full_unstemmed The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon
title_short The human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon
title_sort human jejunum has an endogenous microbiota that differs from those in the oral cavity and colon
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513040/
https://www.ncbi.nlm.nih.gov/pubmed/28716079
http://dx.doi.org/10.1186/s12866-017-1059-6
work_keys_str_mv AT sundinolofh thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT mendozaladdantonio thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT zengmingtao thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT diazarevalodiana thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT moraleselisa thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT faganbmatthew thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT ordonezjavier thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT velezphilip thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT antonynishaal thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT mccallumrichardw thehumanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT sundinolofh humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT mendozaladdantonio humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT zengmingtao humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT diazarevalodiana humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT moraleselisa humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT faganbmatthew humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT ordonezjavier humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT velezphilip humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT antonynishaal humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon
AT mccallumrichardw humanjejunumhasanendogenousmicrobiotathatdiffersfromthoseintheoralcavityandcolon