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Environmental Microbiology

Comparative Genome Analyses of Lactobacillus crispatus Isolates from Different Ecological Niches Reveal an Adaptation of This Species to the Human Vaginal Environment

Leonardo Mancabelli, Walter Mancino, Gabriele Andrea Lugli, Christian Milani, Alice Viappiani, Rosaria Anzalone, Giulia Longhi, Douwe van Sinderen, Marco Ventura, Francesca Turroni
Johanna Björkroth, Editor
Leonardo Mancabelli
aLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy
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Walter Mancino
aLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy
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Gabriele Andrea Lugli
aLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy
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Christian Milani
aLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy
cMicrobiome Research Hub, University of Parma, Parma, Italy
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Alice Viappiani
bGenProbio srl, Parma, Italy
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Rosaria Anzalone
bGenProbio srl, Parma, Italy
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Giulia Longhi
bGenProbio srl, Parma, Italy
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Douwe van Sinderen
dAPC Microbiome Institute and School of Microbiology, Bioscience Institute, National University of Ireland, Cork, Ireland
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Marco Ventura
aLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy
cMicrobiome Research Hub, University of Parma, Parma, Italy
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Francesca Turroni
aLaboratory of Probiogenomics, Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parma, Italy
cMicrobiome Research Hub, University of Parma, Parma, Italy
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Johanna Björkroth
University of Helsinki
Roles: Editor
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DOI: 10.1128/AEM.02899-20
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ABSTRACT

The vaginal microbiota is defined as the community of bacteria residing in the human vaginal tract. Recent studies have demonstrated that the vaginal microbiota is dominated by members of the Lactobacillus genus, whose relative abundance and microbial taxon composition are dependent on the healthy status of this human body site. Particularly, among members of this genus, the high prevalence of Lactobacillus crispatus is commonly associated with a healthy vaginal environment. In the current study, we assessed the microbial composition of 94 healthy vaginal microbiome samples through shotgun metagenomics analyses. Based on our results, we observed that L. crispatus was the most representative species and correlated negatively with bacteria involved in vaginal infections. Therefore, we isolated 15 L. crispatus strains from different environments in which this species abounds, ranging from vaginal swabs of healthy women to chicken fecal samples. The genomes of these strains were decoded and their genetic content was analyzed and correlated with their physiological features. An extensive comparative genomic analysis encompassing all publicly available genome sequences of L. crispatus and combined with those decoded in this study revealed a genetic adaptation of strains to their respective ecological niche. In addition, in vitro growth experiments involving all isolated L. crispatus strains, together with a synthetic vaginal microbiota, reveal how this species is able to modulate the composition of the vaginal microbial consortia at the strain level. Overall, our findings suggest that L. crispatus plays an important ecological role in reducing the complexity of the vaginal microbiota by depleting pathogenic bacteria.

IMPORTANCE The vaginal microbiota is defined as the community of bacteria residing in the human vaginal tract. Recent studies have demonstrated that the high prevalence of Lactobacillus crispatus strains is commonly associated with a healthy vaginal environment. In the current study, we assessed the microbial composition of 94 public healthy vaginal samples through shotgun metagenomics analyses. Results showed that L. crispatus was the most representative species and correlated negatively with bacteria involved in vaginal infections. Moreover, we isolated and sequenced the genomes of new L. crispatus strains from different environments, and the comparative genomics analysis revealed a genetic adaptation of strains to their ecological niche. In addition, in vitro growth experiments display the capability of this species to modulate the composition of the vaginal microbial consortia. Overall, our findings suggest an ecological role exploited by L. crispatus in reducing the complexity of the vaginal microbiota toward a depletion of pathogenic bacteria.

FOOTNOTES

    • Received 26 November 2020.
    • Accepted 3 February 2021.
    • Accepted manuscript posted online 12 February 2021.
  • Supplemental material is available online only.

  • Copyright © 2021 American Society for Microbiology.

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Comparative Genome Analyses of Lactobacillus crispatus Isolates from Different Ecological Niches Reveal an Adaptation of This Species to the Human Vaginal Environment
Leonardo Mancabelli, Walter Mancino, Gabriele Andrea Lugli, Christian Milani, Alice Viappiani, Rosaria Anzalone, Giulia Longhi, Douwe van Sinderen, Marco Ventura, Francesca Turroni
Applied and Environmental Microbiology Mar 2021, 87 (8) e02899-20; DOI: 10.1128/AEM.02899-20

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Comparative Genome Analyses of Lactobacillus crispatus Isolates from Different Ecological Niches Reveal an Adaptation of This Species to the Human Vaginal Environment
Leonardo Mancabelli, Walter Mancino, Gabriele Andrea Lugli, Christian Milani, Alice Viappiani, Rosaria Anzalone, Giulia Longhi, Douwe van Sinderen, Marco Ventura, Francesca Turroni
Applied and Environmental Microbiology Mar 2021, 87 (8) e02899-20; DOI: 10.1128/AEM.02899-20
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KEYWORDS

lactobacilli
vaginal microbiota
comparative genomics

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