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Bacterial vaginosis (BV) is an enigmatic polymicrobial condition characterized by a depletion of health-associated  Lactobacillus  and an overgrowth of anaerobes. Importantly, BV is linked to adverse gynecologic and obstetric outcomes: an increased risk of sexually transmitted infections, preterm birth, and cancer. We hypothesized that members of the cervicovaginal microbiota distinctly contribute to immunometabolic changes in the human cervix, leading to these sequelae. Our 3D epithelial cell model that recapitulates the human cervical epithelium was infected with clinical isolates of cervicovaginal bacteria, alone or as a polymicrobial community. We used  Lactobacillus crispatus  as a representative health-associated commensal and four common BV-associated species:  Gardnerella vaginalis ,  Prevotella bivia ,  Atopobium vaginae , and  Sneathia amnii . The immunometabolic profiles of these microenvironments were analyzed using multiplex immunoassays and untargeted global metabolomics.  A. vaginae  and  S. amnii  exhibited the highest proinflammatory potential through induction of cytokines, iNOS, and oxidative stress-associated compounds.  G. vaginalis ,  P. bivia , and  S. amnii  distinctly altered physicochemical barrier-related proteins and metabolites (mucins, sialic acid, polyamines), whereas  L. crispatus  produced an antimicrobial compound, phenyllactic acid. Alterations to the immunometabolic landscape correlate with symptoms and hallmarks of BV and connected BV with adverse women’s health outcomes. Overall, this study demonstrated that 3D cervical epithelial cell colonized with cervicovaginal microbiota faithfully reproduce the immunometabolic microenvironment previously observed in clinical studies and can successfully be used as a robust tool to evaluate host responses to commensal and pathogenic bacteria in the female reproductive tract.

Bacterial vaginosis and health-associated bacteria modulate the immunometabolic landscape in 3D model of human cervix