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Specific Disruption of Established Pseudomonas aeruginosa Biofilms Using Polymer-Attacking Enzymes

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Download Hi-Res ImageDownload to MS-PowerPointCite This:Langmuir 2020, 36, 6, 1585-1595
    Article

    Specific Disruption of Established Pseudomonas aeruginosa Biofilms Using Polymer-Attacking Enzymes
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    • Kristin N. Kovach
      Kristin N. Kovach
      Department of Physics and Center for Nonlinear Dynamics, The University of Texas at Austin, Austin, Texas 78712, United States
      More by Kristin N. Kovach
    • Derek Fleming
      Derek Fleming
      Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, Texas 79430, United States
      More by Derek Fleming
    • Marilyn J. Wells
      Marilyn J. Wells
      Department of Physics and Center for Nonlinear Dynamics, The University of Texas at Austin, Austin, Texas 78712, United States
      More by Marilyn J. Wells
    • Kendra P. Rumbaugh
      Kendra P. Rumbaugh
      Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, Texas 79430, United States
      More by Kendra P. Rumbaugh
    • Vernita Diane Gordon*
      Vernita Diane Gordon
      Department of Physics and Center for Nonlinear Dynamics, The University of Texas at Austin, Austin, Texas 78712, United States
      Institute for Cellular and Molecular Biology, The University of Texas at Austin, Austin, Texas 78712, United States
      More by Vernita Diane Gordon
      Orcidhttp://orcid.org/0000-0002-5989-9378
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    Langmuir

    Cite this: Langmuir 2020, 36, 6, 1585–1595
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    https://doi.org/10.1021/acs.langmuir.9b02188
    Published January 28, 2020
    Copyright © 2020 American Chemical Society
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    Abstract

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    Biofilms are communities of bacteria embedded in a polymeric matrix which are found in infections and in environments outside the body. Breaking down the matrix renders biofilms more susceptible to physical disruption and to treatments such as antibiotics. Different species of bacteria, and different strains within the same species, produce different types of matrix polymers. This suggests that targeting specific polymers for disruption may be more effective than nonspecific approaches to disrupting biofilm matrixes. In this study, we treated Pseudomonas aeruginosa biofilms with enzymes that are specific to different matrix polymers. We measured the resulting alteration in biofilm mechanics using bulk rheology and changes in structure using electron microscopy. We find that, for biofilms grown in vitro, the effect of enzymatic treatment is greatest when the enzyme is specific to a dominant matrix polymer. Specifically matched enzymatic treatment tends to reduce yield strain and yield stress and increase the rate of biofilm drying, due to increased diffusivity as a result of network compromise. Electron micrographs qualitatively suggest that well-matched enzymatic treatments reduce long-range structure and shorten connecting network fibers. Previous work has shown that generic glycoside hydrolases can cause dispersal of bacteria from in vivo and ex vivo biofilms into a free-swimming state, and thereby make antibiotic treatment more effective. For biofilms grown in wounded mice, we find that well-matched treatments that result in the greatest mechanical compromise in vitro induce the least dispersal ex vivo. Moreover, we find that generic glycoside hydrolases have no measurable effect on the mechanics of biofilms grown in vitro, while previous work has shown them to be highly effective at inducing dispersal in vivo and ex vivo. This highlights the possibility that effective approaches to eradicating biofilms may depend strongly on the growth environment.

    Copyright © 2020 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.langmuir.9b02188.

    • Student two-tailed t tests; G′, yield stress, and yield strain values; SEM images of biofilms; photographs of control and treated biofilms (PDF)

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    Cited By

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    This article is cited by 28 publications.

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    22. Whitni K. Redman, Garrett S. Welch, Avery C. Williams, Addyson J. Damron, Willem O. Northcut, Kendra P. Rumbaugh. Efficacy and safety of biofilm dispersal by glycoside hydrolases in wounds. Biofilm 2021, 3 , 100061. https://doi.org/10.1016/j.bioflm.2021.100061
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    Langmuir

    Cite this: Langmuir 2020, 36, 6, 1585–1595
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.langmuir.9b02188
    Published January 28, 2020
    Copyright © 2020 American Chemical Society
    Request reuse permissions

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