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Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility

Swarmer cells of the Gram-negative uropathogenic bacteria Proteus mirabilis and Vibrio parahaemolyticus become long (>10 to 100 μm) and multinucleate during their growth and motility on polymer surfaces. We demonstrated that the increasing cell length is accompanied by a large increase in flexibi...

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Autores principales: Auer, George K., Oliver, Piercen M., Rajendram, Manohary, Lin, Ti-Yu, Yao, Qing, Jensen, Grant J., Weibel, Douglas B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6786863/
https://www.ncbi.nlm.nih.gov/pubmed/31594808
http://dx.doi.org/10.1128/mBio.00210-19
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author Auer, George K.
Oliver, Piercen M.
Rajendram, Manohary
Lin, Ti-Yu
Yao, Qing
Jensen, Grant J.
Weibel, Douglas B.
author_facet Auer, George K.
Oliver, Piercen M.
Rajendram, Manohary
Lin, Ti-Yu
Yao, Qing
Jensen, Grant J.
Weibel, Douglas B.
author_sort Auer, George K.
collection PubMed
description Swarmer cells of the Gram-negative uropathogenic bacteria Proteus mirabilis and Vibrio parahaemolyticus become long (>10 to 100 μm) and multinucleate during their growth and motility on polymer surfaces. We demonstrated that the 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 the swarmer cell stiffness (bending rigidity) of P. mirabilis (5.5 × 10(−22) N m(2)) and V. parahaemolyticus (1.0 × 10(−22) N m(2)) compared to vegetative cells (1.4 × 10(−20) N m(2) and 2.2 × 10(−22) N m(2), respectively). The reduction in bending rigidity (∼2-fold to ∼26-fold) was accompanied by a decrease in the average polysaccharide strand length of the peptidoglycan layer of the cell wall from 28 to 30 disaccharides to 19 to 22 disaccharides. Atomic force microscopy revealed a reduction in P. mirabilis peptidoglycan thickness from 1.5 nm (vegetative cells) to 1.0 nm (swarmer cells), 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 MICs of the β-lactams cephalexin and penicillin G. The adaptive cost of “swarming” was offset by the increase in cell susceptibility to physical and chemical changes in their environment, thereby suggesting the development of new chemotherapies for bacteria that leverage swarming for the colonization of hosts and for survival.
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spelling pubmed-67868632019-10-15 Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility Auer, George K. Oliver, Piercen M. Rajendram, Manohary Lin, Ti-Yu Yao, Qing Jensen, Grant J. Weibel, Douglas B. mBio Research Article Swarmer cells of the Gram-negative uropathogenic bacteria Proteus mirabilis and Vibrio parahaemolyticus become long (>10 to 100 μm) and multinucleate during their growth and motility on polymer surfaces. We demonstrated that the 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 the swarmer cell stiffness (bending rigidity) of P. mirabilis (5.5 × 10(−22) N m(2)) and V. parahaemolyticus (1.0 × 10(−22) N m(2)) compared to vegetative cells (1.4 × 10(−20) N m(2) and 2.2 × 10(−22) N m(2), respectively). The reduction in bending rigidity (∼2-fold to ∼26-fold) was accompanied by a decrease in the average polysaccharide strand length of the peptidoglycan layer of the cell wall from 28 to 30 disaccharides to 19 to 22 disaccharides. Atomic force microscopy revealed a reduction in P. mirabilis peptidoglycan thickness from 1.5 nm (vegetative cells) to 1.0 nm (swarmer cells), 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 MICs of the β-lactams cephalexin and penicillin G. The adaptive cost of “swarming” was offset by the increase in cell susceptibility to physical and chemical changes in their environment, thereby suggesting the development of new chemotherapies for bacteria that leverage swarming for the colonization of hosts and for survival. American Society for Microbiology 2019-10-08 /pmc/articles/PMC6786863/ /pubmed/31594808 http://dx.doi.org/10.1128/mBio.00210-19 Text en Copyright © 2019 Auer et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Auer, George K.
Oliver, Piercen M.
Rajendram, Manohary
Lin, Ti-Yu
Yao, Qing
Jensen, Grant J.
Weibel, Douglas B.
Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility
title Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility
title_full Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility
title_fullStr Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility
title_full_unstemmed Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility
title_short Bacterial Swarming Reduces Proteus mirabilis and Vibrio parahaemolyticus Cell Stiffness and Increases β-Lactam Susceptibility
title_sort bacterial swarming reduces proteus mirabilis and vibrio parahaemolyticus cell stiffness and increases β-lactam susceptibility
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6786863/
https://www.ncbi.nlm.nih.gov/pubmed/31594808
http://dx.doi.org/10.1128/mBio.00210-19
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