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Unleashing the potential of mRNA-seq to uncover the microbiome structure and their crosstalk with host cells: the vulvar case

ABSTRACT: To comprehensively describe both host gene expression and microbiome composition in a single sample, parallel experimental and computational workflows -mRNA sequencing and either 16S or metagenomics- have been traditionally applied. Here, following in vitro validation of the reliability of Poly(A)-enriched mRNA sequencing in reconstructing the microbiota composition on a defined microbial mock community, we process a cohort of 30 vulvar mRNA-seq samples to fully analyze not only the transcriptome of the vulvar cells, but also the composition of microbial communities and their parallel changes. This three-level analysis on the very same specimens further enables a gene-level exploration of the reciprocal molecular crosstalk between host and microbes. The vulvar milieu represents an area of emerging research for its role in health and disease. Being at the anatomical intersection between the vaginal milieu and the perineal area, the vulvar microbiome displays an intermediate signature, with contamination from both ecosystems. Using this unified framework, we reveal marked heterogeneity and high inter-individual variability in the vulvar microbiota of healthy individuals, identifying community state types that mirror those described in the vaginal ecosystem. Importantly, we show that distinct microbial configurations are associated with specific host transcriptional programs: Lactobacillus crispatus dominated communities correlate with epithelial differentiation and barrier integrity, whereas communities enriched in taxa associated with dysbiosis exhibit transcriptional signatures linked to inflammation. Beyond providing new biological insights into an understudied anatomical niche, our study introduces a broadly applicable strategy with substantial impact for the field. With tens of thousands of human RNA-seq datasets already available in public repositories, our approach enables retrospective extraction of microbiome information and host-microbe interaction signals from existing transcriptomic data, without the need for additional sequencing or specialized microbiome protocols. This unlocks a powerful and cost-effective opportunity to revisit archived RNA-seq studies across tissues, diseases, and low-biomass environments, revealing previously inaccessible layers of host-microbiome crosstalk and maximizing the scientific value of data that already exist.

ORGANISM(S): Homo sapiens

PROVIDER: GSE314734 | GEO | 2026/04/30

REPOSITORIES: GEO

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Project description:Background: While the luminal microbiome composition in the human cervicovaginal tract has been defined, the presence and impact of tissue-adherent ectocervical microbiota remain incompletely understood. Studies of luminal and tissue-associated bacteria in the gastrointestinal tract suggest that they may have distinct roles in health and disease. Here, we performed a multi-omics characterization of paired luminal and tissue samples collected from a clinically well-characterized cohort of Kenyan women. Results: We identified a tissue-adherent bacterial microbiome, with a higher alpha diversity than the luminal microbiome, in which dominant genera overall included Gardnerella and Lactobacillus, followed by Prevotella, Atopobium, and Sneathia. About half of the L. iners dominated luminal samples had a corresponding Gardnerella dominated tissue microbiome. Broadly, the tissue-adherent microbiome was associated with fewer differentially expressed host genes than the luminal microbiome. Gene set enrichment analysis revealed that L. crispatus-dominated tissue-adherent communities were associated with protein translation and antimicrobial activity, whereas a highly diverse microbiome was associated with epithelial remodeling and pro-inflammatory pathways. Communities dominated by L. iners and Gardnerella were associated with low host transcriptional activity. Tissue-adherent microbiomes dominated by Lactobacillus and Gardnerella correlated with host protein profiles associated with epithelial barrier stability, and with a more pro-inflammatory profile for the Gardnerella-dominated microbiome group. Tissue samples with a highly diverse composition had a protein profile representing cell proliferation and pro-inflammatory activity. Conclusion: We identified ectocervical tissue-adherent bacterial communities in all study participants. These communities were distinct from cervicovaginal luminal microbiota in a significant proportion of individuals. This difference could possibly explain that L. iners dominant luminal communities have a high probability of transitioning to high diverse bacterial communities including high abundance of Gardnerella. By performing integrative multi-omics analyses we further revealed that bacterial communities at both sites correlated with distinct host gene expression and protein levels. The tissue-adherent bacterial community is similar to vaginal biofilms that significantly impact women’s reproductive and sexual health.

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Unleashing the potential of mRNA-seq to uncover the microbiome structure and their crosstalk with host cells: the vulvar case

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