Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota.
Women with bacterial vaginosis (BV), an imbalance of the vaginal microbiome, are more likely to be colonized by potential pathogens such as Fusobacterium nucleatum, a bacterium linked with intrauterine infection and preterm birth. However, the conditions and mechanisms supporting pathogen colonizati...
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doaj-b43f4f413fa64ae5b5d56ce5f62edb0d2021-07-02T17:09:26ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852020-08-01188e300078810.1371/journal.pbio.3000788Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota.Kavita AgarwalLloyd S RobinsonSomya AggarwalLynne R FosterAriel Hernandez-LeyvaHueylie LinBrett A TortelliValerie P O'BrienLiza MillerAndrew L KauHilary RenoNicole M GilbertWarren G LewisAmanda L LewisWomen with bacterial vaginosis (BV), an imbalance of the vaginal microbiome, are more likely to be colonized by potential pathogens such as Fusobacterium nucleatum, a bacterium linked with intrauterine infection and preterm birth. However, the conditions and mechanisms supporting pathogen colonization during vaginal dysbiosis remain obscure. We demonstrate that sialidase activity, a diagnostic feature of BV, promoted F. nucleatum foraging and growth on mammalian sialoglycans, a nutrient resource that was otherwise inaccessible because of the lack of endogenous F. nucleatum sialidase. In mice with sialidase-producing vaginal microbiotas, mutant F. nucleatum unable to consume sialic acids was impaired in vaginal colonization. These experiments in mice also led to the discovery that F. nucleatum may also "give back" to the community by reinforcing sialidase activity, a biochemical feature of human dysbiosis. Using human vaginal bacterial communities, we show that F. nucleatum supported robust outgrowth of Gardnerella vaginalis, a major sialidase producer and one of the most abundant organisms in BV. These results illustrate that mutually beneficial relationships between vaginal bacteria support pathogen colonization and may help maintain features of dysbiosis. These findings challenge the simplistic dogma that the mere absence of "healthy" lactobacilli is the sole mechanism that creates a permissive environment for pathogens during vaginal dysbiosis. Given the ubiquity of F. nucleatum in the human mouth, these studies also suggest a possible mechanism underlying links between vaginal dysbiosis and oral sex.https://doi.org/10.1371/journal.pbio.3000788 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Kavita Agarwal Lloyd S Robinson Somya Aggarwal Lynne R Foster Ariel Hernandez-Leyva Hueylie Lin Brett A Tortelli Valerie P O'Brien Liza Miller Andrew L Kau Hilary Reno Nicole M Gilbert Warren G Lewis Amanda L Lewis |
spellingShingle |
Kavita Agarwal Lloyd S Robinson Somya Aggarwal Lynne R Foster Ariel Hernandez-Leyva Hueylie Lin Brett A Tortelli Valerie P O'Brien Liza Miller Andrew L Kau Hilary Reno Nicole M Gilbert Warren G Lewis Amanda L Lewis Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota. PLoS Biology |
author_facet |
Kavita Agarwal Lloyd S Robinson Somya Aggarwal Lynne R Foster Ariel Hernandez-Leyva Hueylie Lin Brett A Tortelli Valerie P O'Brien Liza Miller Andrew L Kau Hilary Reno Nicole M Gilbert Warren G Lewis Amanda L Lewis |
author_sort |
Kavita Agarwal |
title |
Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota. |
title_short |
Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota. |
title_full |
Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota. |
title_fullStr |
Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota. |
title_full_unstemmed |
Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota. |
title_sort |
glycan cross-feeding supports mutualism between fusobacterium and the vaginal microbiota. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS Biology |
issn |
1544-9173 1545-7885 |
publishDate |
2020-08-01 |
description |
Women with bacterial vaginosis (BV), an imbalance of the vaginal microbiome, are more likely to be colonized by potential pathogens such as Fusobacterium nucleatum, a bacterium linked with intrauterine infection and preterm birth. However, the conditions and mechanisms supporting pathogen colonization during vaginal dysbiosis remain obscure. We demonstrate that sialidase activity, a diagnostic feature of BV, promoted F. nucleatum foraging and growth on mammalian sialoglycans, a nutrient resource that was otherwise inaccessible because of the lack of endogenous F. nucleatum sialidase. In mice with sialidase-producing vaginal microbiotas, mutant F. nucleatum unable to consume sialic acids was impaired in vaginal colonization. These experiments in mice also led to the discovery that F. nucleatum may also "give back" to the community by reinforcing sialidase activity, a biochemical feature of human dysbiosis. Using human vaginal bacterial communities, we show that F. nucleatum supported robust outgrowth of Gardnerella vaginalis, a major sialidase producer and one of the most abundant organisms in BV. These results illustrate that mutually beneficial relationships between vaginal bacteria support pathogen colonization and may help maintain features of dysbiosis. These findings challenge the simplistic dogma that the mere absence of "healthy" lactobacilli is the sole mechanism that creates a permissive environment for pathogens during vaginal dysbiosis. Given the ubiquity of F. nucleatum in the human mouth, these studies also suggest a possible mechanism underlying links between vaginal dysbiosis and oral sex. |
url |
https://doi.org/10.1371/journal.pbio.3000788 |
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