Glycan cross-feeding supports mutualism between Fusobacterium and the vaginal microbiota
Open Access
- 25 August 2020
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLoS Biology
- Vol. 18 (8), e3000788
- https://doi.org/10.1371/journal.pbio.3000788
Abstract
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.Keywords
Funding Information
- National Institute of Allergy and Infectious Diseases (R01 AI114635)
- National Institute of Allergy and Infectious Diseases (R01 AI114635)
- National Institute of Allergy and Infectious Diseases (R01 AI127554)
- National Institute of Allergy and Infectious Diseases (K08 AI113184)
- National Institute of Diabetes and Digestive and Kidney Diseases (K01 DK110225)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (F30HD094435)
- Burroughs Wellcome Fund (Preterm Birth Initiative)
- March of Dimes Prematurity Research Center at Washington University (pilot grant)
- Morse Postdoctoral Fellowship
This publication has 111 references indexed in Scilit:
- Metabolic niche of a prominent sulfate-reducing human gut bacteriumProceedings of the National Academy of Sciences of the United States of America, 2013
- Hydrolysis of Secreted Sialoglycoprotein Immunoglobulin A (IgA) in ex Vivo and Biochemical Models of Bacterial VaginosisOnline Journal of Public Health Informatics, 2012
- Bacterial Vaginosis Assessed by Gram Stain and Diminished Colonization Resistance to Incident Gonococcal, Chlamydial, and Trichomonal Genital InfectionThe Journal of Infectious Diseases, 2010
- Global patterns of 16S rRNA diversity at a depth of millions of sequences per sampleProceedings of the National Academy of Sciences of the United States of America, 2010
- Vaginal microbiome of reproductive-age womenProceedings of the National Academy of Sciences of the United States of America, 2010
- Innovations in host and microbial sialic acid biosynthesis revealed by phylogenomic prediction of nonulosonic acid structureProceedings of the National Academy of Sciences of the United States of America, 2009
- Rectal colonization by group B Streptococcus as a predictor of vaginal colonizationAmerican Journal of Obstetrics and Gynecology, 2009
- NeuA Sialic Acid O-Acetylesterase Activity Modulates O-Acetylation of Capsular Polysaccharide in Group B StreptococcusOnline Journal of Public Health Informatics, 2007
- Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT MethodMethods, 2001
- Vaginal indicators of amniotic fluid infection in preterm laborObstetrics & Gynecology, 2001