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Published September 2019 | Submitted + Published + Supplemental Material
Journal Article Open

Bacterial swarming reduces Proteus mirabilis and Vibrio parahaemolyticus cell stiffness and increases β-lactam susceptibility

Abstract

Swarmer cells of the gram-negative pathogenic bacteria Proteus mirabilis and Vibrio parahaemolyticus become long (>10-100 microns) and multinucleate during their growth and motility on polymer surfaces. We demonstrate increasing cell length is accompanied by a large increase in flexibility. Using a microfluidic assay to measure single-cell mechanics, we identified large differences in swarmer cell stiffness of (bending rigidity of P. mirabilis, 9.6 x 10^(-22) N m^2; V. parahaemolyticus, 9.7 x 10^(-23) N m^2) compared to vegetative cells (1.4 x 10^(-20) N m^2 and 3.2 x 10^(-22) N m^2, respectively). The reduction in bending rigidity (~3-15 fold) was accompanied by a decrease in the average polysaccharide strand length of the peptidoglycan layer of the cell wall from 28-30 to 19-22 disaccharides. Atomic force microscopy revealed a reduction in P. mirabilis peptidoglycan thickness from 1.5 nm (vegetative) to 1.0 nm (swarmer) and electron cryotomography indicated changes in swarmer cell wall morphology. P. mirabilis and V. parahaemolyticus swarmer cells became increasingly sensitive to osmotic pressure and susceptible to cell wall-modifying antibiotics (compared to vegetative cells)--they were ~30% more likely to die after 3 h of treatment with minimum inhibitory concentrations of the beta-lactams cephalexin and penicillin G. Long, flexible swarmer cells enables these pathogenic bacteria to form multicellular structures and promotes community motility. The adaptive cost of swarming is offset by a fitness cost in which cells are more susceptible to physical and chemical changes in their environment, thereby suggesting the development of new chemotherapies for bacteria that leverage swarming for survival.

Additional Information

© 2019 Auer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 4 February 2019; Accepted 14 August 2019; Published 8 October 2019. We thank Linda McCarter for V. parahaemolyticus LM5674, Suckjoon Jun for plasmid psulA, Cameron Scarlett and Molly Pellitteri-Hahn for mass spectrometry support, and Julie Last for technical assistance with AFM measurements. This research was supported by the Bill and Melinda Gates Foundation (grant OPP1068092), NIH grant 1DP2OD008735-01, National Science Foundation (NSF) grant DMR-1121288, a Mao Wisconsin Distinguished Graduate Fellowship (to M.R.), an NSF postdoctoral fellowship (no. 1202622 to P.M.O.), and the Howard Hughes Medical Institute.

Attached Files

Published - mBio-2019-Auer-e00210-19.full.pdf

Submitted - 275941.full.pdf

Supplemental Material - 275941-1.pdf

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Created:
August 19, 2023
Modified:
October 20, 2023