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

Auer, George K. and Oliver, Piercen M. and Rajendram, Manohary and Lin, Ti-Yu and Yao, Qing and Jensen, Grant J. and Weibel, Douglas B. (2019) Bacterial swarming reduces Proteus mirabilis and Vibrio parahaemolyticus cell stiffness and increases β-lactam susceptibility. mBio, 10 (5). Art. No. e00210-19. ISSN 2150-7511. PMCID PMC6786863. https://resolver.caltech.edu/CaltechAUTHORS:20181031-082235074

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/mBio.00210-19DOIArticle
https://doi.org/10.1101/275941DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6786863/PubMed CentralArticle
ORCID:
AuthorORCID
Yao, Qing0000-0003-3575-9909
Jensen, Grant J.0000-0003-1556-4864
Weibel, Douglas B.0000-0001-7797-2017
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.
Funders:
Funding AgencyGrant Number
Bill and Melinda Gates FoundationOPP1068092
NIH1DP2OD008735-01
NSFDMR-1121288
University of Wisconsin-MadisonUNSPECIFIED
NSF Postdoctoral FellowshipDBI-1202622
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:antibiotics, bacterial cell mechanics, bacterial swarming, osmotic pressure, peptidoglycan
Issue or Number:5
PubMed Central ID:PMC6786863
Record Number:CaltechAUTHORS:20181031-082235074
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181031-082235074
Official Citation:Auer GK, Oliver PM, Rajendram M, Lin T-Y, Yao Q, Jensen GJ, Weibel DB. 2019. Bacterial swarming reduces Proteus mirabilis and Vibrio parahaemolyticus cell stiffness and increases β-lactam susceptibility. mBio 10:e00210-19. https://doi.org/10.1128/mBio.00210-19
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90533
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Nov 2018 18:27
Last Modified:05 Nov 2019 18:13

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