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Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data

BACKGROUND: Vaginal bacterial communities dominated by Lactobacillus species are associated with a reduced risk of various adverse health outcomes. However, somewhat unexpectedly, many healthy women have microbiota that are not dominated by lactobacilli. To determine the factors that drive vaginal c...

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Autores principales: France, Michael T., Fu, Li, Rutt, Lindsay, Yang, Hongqiu, Humphrys, Michael S., Narina, Shilpa, Gajer, Pawel M., Ma, Bing, Forney, Larry J., Ravel, Jacques
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8886902/
https://www.ncbi.nlm.nih.gov/pubmed/35232471
http://dx.doi.org/10.1186/s13059-022-02635-9
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author France, Michael T.
Fu, Li
Rutt, Lindsay
Yang, Hongqiu
Humphrys, Michael S.
Narina, Shilpa
Gajer, Pawel M.
Ma, Bing
Forney, Larry J.
Ravel, Jacques
author_facet France, Michael T.
Fu, Li
Rutt, Lindsay
Yang, Hongqiu
Humphrys, Michael S.
Narina, Shilpa
Gajer, Pawel M.
Ma, Bing
Forney, Larry J.
Ravel, Jacques
author_sort France, Michael T.
collection PubMed
description BACKGROUND: Vaginal bacterial communities dominated by Lactobacillus species are associated with a reduced risk of various adverse health outcomes. However, somewhat unexpectedly, many healthy women have microbiota that are not dominated by lactobacilli. To determine the factors that drive vaginal community composition we characterized the genetic composition and transcriptional activities of vaginal microbiota in healthy women. RESULTS: We demonstrate that the abundance of a species is not always indicative of its transcriptional activity and that impending changes in community composition can be predicted from metatranscriptomic data. Functional comparisons highlight differences in the metabolic activities of these communities, notably in their degradation of host produced mucin but not glycogen. Degradation of mucin by communities not dominated by Lactobacillus may play a role in their association with adverse health outcomes. Finally, we show that the transcriptional activities of L. crispatus, L. iners, and Gardnerella vaginalis vary with the taxonomic composition of the communities in which they reside. Notably, L. iners and G. vaginalis both demonstrate lower expression of their cholesterol-dependent cytolysins when co-resident with Lactobacillus spp. and higher expression when co-resident with other facultative and obligate anaerobes. The pathogenic potential of these species may depend on the communities in which they reside and thus could be modulated by interventional strategies. CONCLUSIONS: Our results provide insight to the functional ecology of the vaginal microbiota, demonstrate the diagnostic potential of metatranscriptomic data, and reveal strategies for the management of these ecosystems. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02635-9.
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spelling pubmed-88869022022-03-17 Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data France, Michael T. Fu, Li Rutt, Lindsay Yang, Hongqiu Humphrys, Michael S. Narina, Shilpa Gajer, Pawel M. Ma, Bing Forney, Larry J. Ravel, Jacques Genome Biol Research BACKGROUND: Vaginal bacterial communities dominated by Lactobacillus species are associated with a reduced risk of various adverse health outcomes. However, somewhat unexpectedly, many healthy women have microbiota that are not dominated by lactobacilli. To determine the factors that drive vaginal community composition we characterized the genetic composition and transcriptional activities of vaginal microbiota in healthy women. RESULTS: We demonstrate that the abundance of a species is not always indicative of its transcriptional activity and that impending changes in community composition can be predicted from metatranscriptomic data. Functional comparisons highlight differences in the metabolic activities of these communities, notably in their degradation of host produced mucin but not glycogen. Degradation of mucin by communities not dominated by Lactobacillus may play a role in their association with adverse health outcomes. Finally, we show that the transcriptional activities of L. crispatus, L. iners, and Gardnerella vaginalis vary with the taxonomic composition of the communities in which they reside. Notably, L. iners and G. vaginalis both demonstrate lower expression of their cholesterol-dependent cytolysins when co-resident with Lactobacillus spp. and higher expression when co-resident with other facultative and obligate anaerobes. The pathogenic potential of these species may depend on the communities in which they reside and thus could be modulated by interventional strategies. CONCLUSIONS: Our results provide insight to the functional ecology of the vaginal microbiota, demonstrate the diagnostic potential of metatranscriptomic data, and reveal strategies for the management of these ecosystems. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-022-02635-9. BioMed Central 2022-03-01 /pmc/articles/PMC8886902/ /pubmed/35232471 http://dx.doi.org/10.1186/s13059-022-02635-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
France, Michael T.
Fu, Li
Rutt, Lindsay
Yang, Hongqiu
Humphrys, Michael S.
Narina, Shilpa
Gajer, Pawel M.
Ma, Bing
Forney, Larry J.
Ravel, Jacques
Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
title Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
title_full Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
title_fullStr Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
title_full_unstemmed Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
title_short Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
title_sort insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8886902/
https://www.ncbi.nlm.nih.gov/pubmed/35232471
http://dx.doi.org/10.1186/s13059-022-02635-9
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