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A 'rich-get-richer' mechanism drives patchy dynamics and resistance evolution in antibiotic-treated bacteria.

Publication ,  Journal Article
Şimşek, E; Kim, K; Lu, J; Silver, A; Luo, N; Lee, CT; You, L
Published in: Molecular systems biology
August 2024

Bacteria in nature often form surface-attached communities that initially comprise distinct subpopulations, or patches. For pathogens, these patches can form at infection sites, persist during antibiotic treatment, and develop into mature biofilms. Evidence suggests that patches can emerge due to heterogeneity in the growth environment and bacterial seeding, as well as cell-cell signaling. However, it is unclear how these factors contribute to patch formation and how patch formation might affect bacterial survival and evolution. Here, we demonstrate that a 'rich-get-richer' mechanism drives patch formation in bacteria exhibiting collective survival (CS) during antibiotic treatment. Modeling predicts that the seeding heterogeneity of these bacteria is amplified by local CS and global resource competition, leading to patch formation. Increasing the dose of a non-eradicating antibiotic treatment increases the degree of patchiness. Experimentally, we first demonstrated the mechanism using engineered Escherichia coli and then demonstrated its applicability to a pathogen, Pseudomonas aeruginosa. We further showed that the formation of P. aeruginosa patches promoted the evolution of antibiotic resistance. Our work provides new insights into population dynamics and resistance evolution during surface-attached bacterial growth.

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Published In

Molecular systems biology

DOI

EISSN

1744-4292

ISSN

1744-4292

Publication Date

August 2024

Volume

20

Issue

8

Start / End Page

880 / 897

Related Subject Headings

  • Pseudomonas aeruginosa
  • Models, Biological
  • Escherichia coli
  • Drug Resistance, Bacterial
  • Biological Evolution
  • Bioinformatics
  • Biofilms
  • Anti-Bacterial Agents
  • 3101 Biochemistry and cell biology
  • 0699 Other Biological Sciences
 

Citation

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Şimşek, E., Kim, K., Lu, J., Silver, A., Luo, N., Lee, C. T., & You, L. (2024). A 'rich-get-richer' mechanism drives patchy dynamics and resistance evolution in antibiotic-treated bacteria. Molecular Systems Biology, 20(8), 880–897. https://doi.org/10.1038/s44320-024-00046-5
Şimşek, Emrah, Kyeri Kim, Jia Lu, Anita Silver, Nan Luo, Charlotte T. Lee, and Lingchong You. “A 'rich-get-richer' mechanism drives patchy dynamics and resistance evolution in antibiotic-treated bacteria.Molecular Systems Biology 20, no. 8 (August 2024): 880–97. https://doi.org/10.1038/s44320-024-00046-5.
Şimşek E, Kim K, Lu J, Silver A, Luo N, Lee CT, et al. A 'rich-get-richer' mechanism drives patchy dynamics and resistance evolution in antibiotic-treated bacteria. Molecular systems biology. 2024 Aug;20(8):880–97.
Şimşek, Emrah, et al. “A 'rich-get-richer' mechanism drives patchy dynamics and resistance evolution in antibiotic-treated bacteria.Molecular Systems Biology, vol. 20, no. 8, Aug. 2024, pp. 880–97. Epmc, doi:10.1038/s44320-024-00046-5.
Şimşek E, Kim K, Lu J, Silver A, Luo N, Lee CT, You L. A 'rich-get-richer' mechanism drives patchy dynamics and resistance evolution in antibiotic-treated bacteria. Molecular systems biology. 2024 Aug;20(8):880–897.
Journal cover image

Published In

Molecular systems biology

DOI

EISSN

1744-4292

ISSN

1744-4292

Publication Date

August 2024

Volume

20

Issue

8

Start / End Page

880 / 897

Related Subject Headings

  • Pseudomonas aeruginosa
  • Models, Biological
  • Escherichia coli
  • Drug Resistance, Bacterial
  • Biological Evolution
  • Bioinformatics
  • Biofilms
  • Anti-Bacterial Agents
  • 3101 Biochemistry and cell biology
  • 0699 Other Biological Sciences