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Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa
Improving our understanding of host–microbe relationships in the gut requires the ability to both visualize and quantify the spatial organization of microbial communities in their native orientation with the host tissue. We developed a systematic procedure to quantify the three-dimensional (3D) spat...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9171773/ https://www.ncbi.nlm.nih.gov/pubmed/35476531 http://dx.doi.org/10.1073/pnas.2118483119 |
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author | Mondragón-Palomino, Octavio Poceviciute, Roberta Lignell, Antti Griffiths, Jessica A. Takko, Heli Ismagilov, Rustem F. |
author_facet | Mondragón-Palomino, Octavio Poceviciute, Roberta Lignell, Antti Griffiths, Jessica A. Takko, Heli Ismagilov, Rustem F. |
author_sort | Mondragón-Palomino, Octavio |
collection | PubMed |
description | Improving our understanding of host–microbe relationships in the gut requires the ability to both visualize and quantify the spatial organization of microbial communities in their native orientation with the host tissue. We developed a systematic procedure to quantify the three-dimensional (3D) spatial structure of the native mucosal microbiota in any part of the intestines with taxonomic and high spatial resolution. We performed a 3D biogeographical analysis of the microbiota of mouse cecal crypts at different stages of antibiotic exposure. By tracking eubacteria and four dominant bacterial taxa, we found that the colonization of crypts by native bacteria is a dynamic and spatially organized process. Ciprofloxacin treatment drastically reduced bacterial loads and eliminated Muribaculaceae (or all Bacteroidetes entirely) even 10 d after recovery when overall bacterial loads returned to preantibiotic levels. Our 3D quantitative imaging approach revealed that the bacterial colonization of crypts is organized in a spatial pattern that consists of clusters of adjacent colonized crypts that are surrounded by unoccupied crypts, and that this spatial pattern is resistant to the elimination of Muribaculaceae or of all Bacteroidetes by ciprofloxacin. Our approach also revealed that the composition of cecal crypt communities is diverse and that Lactobacilli were found closer to the lumen than Bacteroidetes, Ruminococcaceae, and Lachnospiraceae, regardless of antibiotic exposure. Finally, we found that crypts communities with similar taxonomic composition were physically closer to each other than communities that were taxonomically different. |
format | Online Article Text |
id | pubmed-9171773 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-91717732022-06-08 Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa Mondragón-Palomino, Octavio Poceviciute, Roberta Lignell, Antti Griffiths, Jessica A. Takko, Heli Ismagilov, Rustem F. Proc Natl Acad Sci U S A Biological Sciences Improving our understanding of host–microbe relationships in the gut requires the ability to both visualize and quantify the spatial organization of microbial communities in their native orientation with the host tissue. We developed a systematic procedure to quantify the three-dimensional (3D) spatial structure of the native mucosal microbiota in any part of the intestines with taxonomic and high spatial resolution. We performed a 3D biogeographical analysis of the microbiota of mouse cecal crypts at different stages of antibiotic exposure. By tracking eubacteria and four dominant bacterial taxa, we found that the colonization of crypts by native bacteria is a dynamic and spatially organized process. Ciprofloxacin treatment drastically reduced bacterial loads and eliminated Muribaculaceae (or all Bacteroidetes entirely) even 10 d after recovery when overall bacterial loads returned to preantibiotic levels. Our 3D quantitative imaging approach revealed that the bacterial colonization of crypts is organized in a spatial pattern that consists of clusters of adjacent colonized crypts that are surrounded by unoccupied crypts, and that this spatial pattern is resistant to the elimination of Muribaculaceae or of all Bacteroidetes by ciprofloxacin. Our approach also revealed that the composition of cecal crypt communities is diverse and that Lactobacilli were found closer to the lumen than Bacteroidetes, Ruminococcaceae, and Lachnospiraceae, regardless of antibiotic exposure. Finally, we found that crypts communities with similar taxonomic composition were physically closer to each other than communities that were taxonomically different. National Academy of Sciences 2022-04-27 2022-05-03 /pmc/articles/PMC9171773/ /pubmed/35476531 http://dx.doi.org/10.1073/pnas.2118483119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Biological Sciences Mondragón-Palomino, Octavio Poceviciute, Roberta Lignell, Antti Griffiths, Jessica A. Takko, Heli Ismagilov, Rustem F. Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa |
title | Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa |
title_full | Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa |
title_fullStr | Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa |
title_full_unstemmed | Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa |
title_short | Three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa |
title_sort | three-dimensional imaging for the quantification of spatial patterns in microbiota of the intestinal mucosa |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9171773/ https://www.ncbi.nlm.nih.gov/pubmed/35476531 http://dx.doi.org/10.1073/pnas.2118483119 |
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