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.

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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

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article

Gut epithelial electrical cues drive differential localization of enterobacteria

Min Zhao, Brian Reid, Renée M. Tsolis, Kan Zhu et al.
11 citations
Nature Microbiology
Planarian Biology and Electrostimulation
2.57
article

Gut epithelial electrical cues drive differential localization of enterobacteria

Min Zhao, Brian Reid, Renée M. Tsolis, Kan Zhu, Li Ma, Fernando Ferreira, Yaohui Sun, Alex Mogilner, Catherine E. Hagan, Briana M. Young
article en
11 citations

Abstract

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.

Nature MicrobiologyVol. 9(10)
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)
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
Openalex Percentile: Top 10%
Planarian Biology and Electrostimulation
2.57
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