Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial cultures
Abstract Background The microbiome regulates the respiratory epithelium’s immunomodulatory functions. To explore how the microbiome’s biodiversity affects microbe-epithelial interactions, we screened 58 phylogenetically diverse microbes for their transcriptomic effect on human primary bronchial air–...
Saved in:
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2025-01-01
|
| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-025-02129-7 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832571291205369856 |
|---|---|
| author | Mian Horvath Ruoyu Yang Diana Cadena Castaneda Megan Callender Elizabeth S. Aiken Anita Y. Voigt Ryan Caldwell José Fachi Blanda Di Luccia Zoe Scholar Peter Yu Andrew Salner Marco Colonna Karolina Palucka Julia Oh |
| author_facet | Mian Horvath Ruoyu Yang Diana Cadena Castaneda Megan Callender Elizabeth S. Aiken Anita Y. Voigt Ryan Caldwell José Fachi Blanda Di Luccia Zoe Scholar Peter Yu Andrew Salner Marco Colonna Karolina Palucka Julia Oh |
| author_sort | Mian Horvath |
| collection | DOAJ |
| description | Abstract Background The microbiome regulates the respiratory epithelium’s immunomodulatory functions. To explore how the microbiome’s biodiversity affects microbe-epithelial interactions, we screened 58 phylogenetically diverse microbes for their transcriptomic effect on human primary bronchial air–liquid interface (ALI) cell cultures. Results We found distinct species- and strain-level differences in host innate immunity and epithelial barrier response. Strikingly, we found that host interferon, an antiviral response, was one of the most variable host processes. This variability was not driven by microbial phylogenetic diversity, bioburden, nor by the microbe’s ability to stimulate other innate immunity pathways. Conclusions Microbial colonization differentially stimulates host gene expression with variations observed across phylogenetically diverse microbes and across different strains of the same species. Our study provides a foundation for understanding how the respiratory microbiome’s biodiversity affects epithelial, and particularly antiviral, innate immunity. |
| format | Article |
| id | doaj-art-30c96d4f84c84f0d94802ca69946bd53 |
| institution | Kabale University |
| issn | 1741-7007 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj-art-30c96d4f84c84f0d94802ca69946bd532025-02-02T12:42:39ZengBMCBMC Biology1741-70072025-01-0123112310.1186/s12915-025-02129-7Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial culturesMian Horvath0Ruoyu Yang1Diana Cadena Castaneda2Megan Callender3Elizabeth S. Aiken4Anita Y. Voigt5Ryan Caldwell6José Fachi7Blanda Di Luccia8Zoe Scholar9Peter Yu10Andrew Salner11Marco Colonna12Karolina Palucka13Julia Oh14The Jackson Laboratory for Genomic MedicineThe Jackson Laboratory for Genomic MedicineThe Jackson Laboratory for Genomic MedicineThe Jackson Laboratory for Genomic MedicineThe Jackson Laboratory for Genomic MedicineThe Jackson Laboratory for Genomic MedicineThe Jackson Laboratory for Genomic MedicineWashington University School of MedicineWashington University School of MedicineThe Jackson Laboratory for Genomic MedicineHartford Healthcare Cancer InstituteHartford Healthcare Cancer InstituteWashington University School of MedicineThe Jackson Laboratory for Genomic MedicineThe Jackson Laboratory for Genomic MedicineAbstract Background The microbiome regulates the respiratory epithelium’s immunomodulatory functions. To explore how the microbiome’s biodiversity affects microbe-epithelial interactions, we screened 58 phylogenetically diverse microbes for their transcriptomic effect on human primary bronchial air–liquid interface (ALI) cell cultures. Results We found distinct species- and strain-level differences in host innate immunity and epithelial barrier response. Strikingly, we found that host interferon, an antiviral response, was one of the most variable host processes. This variability was not driven by microbial phylogenetic diversity, bioburden, nor by the microbe’s ability to stimulate other innate immunity pathways. Conclusions Microbial colonization differentially stimulates host gene expression with variations observed across phylogenetically diverse microbes and across different strains of the same species. Our study provides a foundation for understanding how the respiratory microbiome’s biodiversity affects epithelial, and particularly antiviral, innate immunity.https://doi.org/10.1186/s12915-025-02129-7Respiratory microbiomeBacteriaEpitheliumInterferonAntiviral immunityRNA-seq |
| spellingShingle | Mian Horvath Ruoyu Yang Diana Cadena Castaneda Megan Callender Elizabeth S. Aiken Anita Y. Voigt Ryan Caldwell José Fachi Blanda Di Luccia Zoe Scholar Peter Yu Andrew Salner Marco Colonna Karolina Palucka Julia Oh Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial cultures BMC Biology Respiratory microbiome Bacteria Epithelium Interferon Antiviral immunity RNA-seq |
| title | Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial cultures |
| title_full | Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial cultures |
| title_fullStr | Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial cultures |
| title_full_unstemmed | Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial cultures |
| title_short | Species- and strain-specific microbial modulation of interferon, innate immunity, and epithelial barrier in 2D air–liquid interface respiratory epithelial cultures |
| title_sort | species and strain specific microbial modulation of interferon innate immunity and epithelial barrier in 2d air liquid interface respiratory epithelial cultures |
| topic | Respiratory microbiome Bacteria Epithelium Interferon Antiviral immunity RNA-seq |
| url | https://doi.org/10.1186/s12915-025-02129-7 |
| work_keys_str_mv | AT mianhorvath speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT ruoyuyang speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT dianacadenacastaneda speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT megancallender speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT elizabethsaiken speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT anitayvoigt speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT ryancaldwell speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT josefachi speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT blandadiluccia speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT zoescholar speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT peteryu speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT andrewsalner speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT marcocolonna speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT karolinapalucka speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures AT juliaoh speciesandstrainspecificmicrobialmodulationofinterferoninnateimmunityandepithelialbarrierin2dairliquidinterfacerespiratoryepithelialcultures |