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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...

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Autores principales: Mondragón-Palomino, Octavio, Poceviciute, Roberta, Lignell, Antti, Griffiths, Jessica A., Takko, Heli, Ismagilov, Rustem F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
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.
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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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