The role of bacterial size, shape and surface in macrophage engulfment of uropathogenic E. coli cells

Uropathogenic Escherichia coli (UPEC) can undergo extensive filamentation in the host during acute urinary tract infections (UTIs). It has been hypothesised that this morphological plasticity allows bacteria to avoid host immune responses such as macrophage engulfment. However, it is still unclear what properties of filaments are important in macrophage-bacteria interactions. The aim of this work was to investigate the contribution of bacterial biophysical parameters, such as cell size and shape, and physiological parameters, such as cell surface and the environment, to macrophage engulfment efficiency. Viable, reversible filaments of known lengths and volumes were produced in the UPEC strain UTI89 using a variety of methods, including exposure to cell-wall targeting antibiotics, genetic manipulation and isolation from an in vitro human bladder cell model. Quantification of the engulfment ability of macrophages using gentamicin-protection assays and fluorescence microscopy demonstrated that the ability of filaments to avoid macrophage engulfment is dependent on a combination of size (length and volume), shape, cell surface and external environmental factors. UTI89 filamentation and macrophage engulfment efficiency were also found to occur independently of the SOS-inducible filamentation genes, sulA and ymfM in both in vivo and in vitro models of infection. Compared to filaments formed via antibiotic inhibition of division, the infection-derived filaments were preferentially targeted by macrophages. With several strains of UPEC now resistant to current antibiotics, our work identifies the importance of bacterial physiological and morphological states during infection.

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Publication Details

Journal
PLoS Pathogens
Published
2024-09-06
DOI
https://doi.org/10.1371/journal.ppat.1012458
Citations
12
Primary Topic
Urinary Tract Infections Management
Type
article
Field-Weighted Citation Impact
4.64

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article

The role of bacterial size, shape and surface in macrophage engulfment of uropathogenic E. coli cells

Gregory Iosifidis, Rasmus Birkholm Grønnemose, Giang H.B. Le, Bill Söderström et al.
12 citations
PLoS Pathogens
Urinary Tract Infections Management
4.64
article

The role of bacterial size, shape and surface in macrophage engulfment of uropathogenic E. coli cells

Gregory Iosifidis, Rasmus Birkholm Grønnemose, Giang H.B. Le, Bill Söderström, Lauren E. Hartley‐Tassell, Elizabeth Peterson, Bernadette M. Saunders, Christian Evenhuis, Amy L. Bottomley, Jakob Møller‐Jensen, Elizabeth J. Harry, Nienke Prins, Thomas Emil Andersen, Iain G. Duggin
article en
12 citations

Abstract

Uropathogenic Escherichia coli (UPEC) can undergo extensive filamentation in the host during acute urinary tract infections (UTIs). It has been hypothesised that this morphological plasticity allows bacteria to avoid host immune responses such as macrophage engulfment. However, it is still unclear what properties of filaments are important in macrophage-bacteria interactions. The aim of this work was to investigate the contribution of bacterial biophysical parameters, such as cell size and shape, and physiological parameters, such as cell surface and the environment, to macrophage engulfment efficiency. Viable, reversible filaments of known lengths and volumes were produced in the UPEC strain UTI89 using a variety of methods, including exposure to cell-wall targeting antibiotics, genetic manipulation and isolation from an in vitro human bladder cell model. Quantification of the engulfment ability of macrophages using gentamicin-protection assays and fluorescence microscopy demonstrated that the ability of filaments to avoid macrophage engulfment is dependent on a combination of size (length and volume), shape, cell surface and external environmental factors. UTI89 filamentation and macrophage engulfment efficiency were also found to occur independently of the SOS-inducible filamentation genes, sulA and ymfM in both in vivo and in vitro models of infection. Compared to filaments formed via antibiotic inhibition of division, the infection-derived filaments were preferentially targeted by macrophages. With several strains of UPEC now resistant to current antibiotics, our work identifies the importance of bacterial physiological and morphological states during infection.

PLoS PathogensVol. 20(9)
University of Technology Sydney (AU), Griffith University (AU), University of Southern Denmark (DK), Odense University Hospital (DK)
Australian Government, University of Technology Sydney, Australian Research Council
Life in Land
Openalex Percentile: Top 4%
Urinary Tract Infections Management
4.64
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