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

View ORCID ProfileM. T. France, L. Fu, L. Rutt, H. Yang, M. Humphrys, S. Narina, P. Gajer, View ORCID ProfileB. Ma, L. J. Forney, View ORCID ProfileJ. Ravel
doi: https://doi.org/10.1101/2021.06.17.448822
M. T. France
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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L. Fu
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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L. Rutt
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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H. Yang
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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M. Humphrys
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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S. Narina
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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P. Gajer
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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B. Ma
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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L. J. Forney
2Institute for Bioinformatics and Evolutionary Studies and Department of Biology, University of Idaho, Moscow, ID USA
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J. Ravel
1Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD USA
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  • For correspondence: jravel@som.umaryland.edu
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Abstract

Vaginal bacterial communities dominated by Lactobacillus species are associated with a reduced risk to 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. We demonstrated 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 G. vaginalis vary with the taxonomic composition of the communities in which they reside. Notably, L. iners and G. vaginalis both demonstrated 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. Our results provide insight to the functional ecology of vaginal microbiota and reveal strategies for management of these ecosystems.

Competing Interest Statement

J.R. is a cofounder of LUCA Biologics, a biotechnology company focusing on translating microbiome research into live biotherapeutic drugs for women's health. All other authors declare no competing interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 17, 2021.
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Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
M. T. France, L. Fu, L. Rutt, H. Yang, M. Humphrys, S. Narina, P. Gajer, B. Ma, L. J. Forney, J. Ravel
bioRxiv 2021.06.17.448822; doi: https://doi.org/10.1101/2021.06.17.448822
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Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data
M. T. France, L. Fu, L. Rutt, H. Yang, M. Humphrys, S. Narina, P. Gajer, B. Ma, L. J. Forney, J. Ravel
bioRxiv 2021.06.17.448822; doi: https://doi.org/10.1101/2021.06.17.448822

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