Gut epithelial electrical cues drive differential localization of enterobacteria
Salmonella translocate to the gut epithelium via microfold cells lining the follicle-associated epithelium (FAE). How Salmonella localize to the FAE is not well characterized. Here we use live imaging and competitive assays between wild-type and chemotaxis-deficient mutants to show that Salmonella enterica serotype Typhimurium (S. Typhimurium) localize to the FAE independently of chemotaxis in an ex vivo mouse caecum infection model. Electrical recordings revealed polarized FAE with sustained outward current and small transepithelial potential, while the surrounding villus is depolarized with inward current and large transepithelial potential. The distinct electrical potentials attracted S. Typhimurium to the FAE while Escherichia coli (E. coli) localized to the villi, through a process called galvanotaxis. Chloride flux involving the cystic fibrosis transmembrane conductance regulator (CFTR) generated the ionic currents around the FAE. Pharmacological inhibition of CFTR decreased S. Typhimurium FAE localization but increased E. coli recruitment. Altogether, our findings demonstrate that bioelectric cues contribute to S. Typhimurium targeting of specific gut epithelial locations, with potential implications for other enteric bacterial infections.
Authors
- Min Zhao (ORCID: https://orcid.org/0000-0002-2500-3035)
- Brian Reid (ORCID: https://orcid.org/0000-0003-2966-1251)
- Renée M. Tsolis (ORCID: https://orcid.org/0000-0001-9131-6657)
- Kan Zhu (ORCID: https://orcid.org/0000-0002-1146-8130)
- Li Ma (ORCID: https://orcid.org/0000-0002-5551-707X)
- Fernando Ferreira (ORCID: https://orcid.org/0000-0001-5786-8896)
- Yaohui Sun (ORCID: https://orcid.org/0000-0002-3716-6659)
- Alex Mogilner (ORCID: https://orcid.org/0000-0002-9310-3812)
- Catherine E. Hagan (ORCID: https://orcid.org/0000-0001-6831-9921)
- Briana M. Young
Institutions
- University of Washington (US)
- Shanghai Innovative Research Center of Traditional Chinese Medicine (CN)
- University of California System (US)
- Courant Institute of Mathematical Sciences (US)
- New York University (US)
- University of California, Davis (US)
- University of Minho (PT)
Publication Details
- Journal
- Nature Microbiology
- Published
- 2024-08-20
- DOI
- https://doi.org/10.1038/s41564-024-01778-8
- Citations
- 11
- Primary Topic
- Planarian Biology and Electrostimulation
- Type
- article
- Field-Weighted Citation Impact
- 2.57
Funders
- National Institutes of Health
- Defense Advanced Research Projects Agency
- Advanced Research Projects Agency
- Multidisciplinary University Research Initiative
- Fundação para a Ciência e a Tecnologia
- National Eye Institute
- Air Force Office of Scientific Research