Improved microscopic dynamics in mucus gels under mechanical load in the linear viscoelastic regime

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Importance

Mucus is a biological gel that protects several tissues. Its key properties result from a crucial balance between solid-like and fluid-like behavior, provided by the non-permanent nature of the bonds between its macromolecular constituents. Our understanding of the microscale response of mucus to applied stress is still rudimentary, although in living organisms, stresses acting on mucus are ubiquitous, from bacterial penetration to coughing and peristalsis. We show that under a modest applied stress, in the mechanical linear regime, the microscopic dynamics of pig gastric mucus transiently accelerates up to 2 orders of magnitude. A simple model rationalizes this hitherto unrecognized fluidization mechanism resulting from elastic recoil after bond breakage and generalizes our results to networks with reversible bonds.

Abstract

Mucus is a biological gel that covers the surface of several tissues and performs key biological functions, including as a protective barrier against dehydration, penetration of pathogens or stomach acids. The biological functioning of mucus requires a finely tuned balance between a mechanical response of the solid and fluid type, provided by reversible bonds between the mucins, the glycoproteins which form the gel. In living organisms, mucus is subjected to various types of mechanical stress, for example due to osmosis, bacterial penetration, coughing and gastric peristalsis. However, our knowledge of the effects of stress on mucus is still rudimentary and mainly limited to macroscopic rheological measurements, without any insight into the relevant microscopic mechanisms. Here, we perform mechanical tests simultaneously with measurements of the microscopic dynamics of pig gastric mucus. Strikingly, we find that a modest shear stress, in the linear rheological macroscopic regime, significantly improves the reorganization of mucus at the microscopic level, as indicated by a transient acceleration of the microscopic dynamics, up to 2 orders of magnitude. We rationalize these results by proposing a simple but general model for the dynamics of physical gels under stress and validate its hypotheses by numerical simulations of spring networks. These results shed light on the dynamics of mucus rearrangement on a microscopic scale, with potential implications in phenomena ranging from mucus clearance to bacterial and drug penetration.

Footnotes

    • Accepted September 19, 2021.
  • Author contributions: research designed by DL and LC; DL, AP, A.-MP and LC carried out research; MYN contributed to the model; Data analyzed by DL, AP, MYN and LC; and DL and LC wrote the article.

  • The authors declare no competing interests.

  • This article is a direct PNAS submission.

  • This article contains additional information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2103995118/-/DCSupplemental.

Data availability

ASCII and Excel files for all data sets shown in the main text figures and SI Annex were deposited at Zenodo (DOI: 10.5281 / zenodo.5533877) (74).


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