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Evidence for biosurfactant-induced flow in corners and bacterial spreading in unsaturated porous media - pnas.org

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Significance

Here, we demonstrate a previously unreported mechanism of bacterial spreading in unsaturated porous media, which can inform understanding of soil contamination by pathogens, soft rot in plants, and potentially many pulmonary diseases. We discover that surfactant-producing bacteria establish self-generated flows along corners by producing surfactants that change the wettability of the solid surface. We validate this corner flow mechanism in a model of soil consisting of packed grains. These results provide a mechanistic explanation for observations that the spread of bacteria increases with increasing surfactants in soil and plants. The biosurfactant-driven corner flow has an average velocity of millimeters per hour, which is significant in terms of the spread of bacteria (e.g., pathogens) in soil and other unsaturated porous media.

Abstract

The spread of pathogenic bacteria in unsaturated porous media, where air and liquid coexist in pore spaces, is the major cause of soil contamination by pathogens, soft rot in plants, food spoilage, and many pulmonary diseases. However, visualization and fundamental understanding of bacterial transport in unsaturated porous media are currently lacking, limiting the ability to address the above contamination- and disease-related issues. Here, we demonstrate a previously unreported mechanism by which bacterial cells are transported in unsaturated porous media. We discover that surfactant-producing bacteria can generate flows along corners through surfactant production that changes the wettability of the solid surface. The corner flow velocity is on the order of several millimeters per hour, which is the same order of magnitude as bacterial swarming, one of the fastest known modes of bacterial surface translocation. We successfully predict the critical corner angle for bacterial corner flow to occur based on the biosurfactant-induced change in the contact angle of the bacterial solution on the solid surface. Furthermore, we demonstrate that bacteria can indeed spread by producing biosurfactants in a model soil, which consists of packed angular grains. In addition, we demonstrate that bacterial corner flow is controlled by quorum sensing, the cell–cell communication process that regulates biosurfactant production. Understanding this previously unappreciated bacterial transport mechanism will enable more accurate predictions of bacterial spreading in soil and other unsaturated porous media.

Footnotes

  • Author contributions: J.Q.Y. designed research; J.Q.Y. and N.A. performed research; J.E.S. and Z.G. contributed new reagents/analytic tools; J.Q.Y., B.L.B., and H.A.S. analyzed data; and J.Q.Y. and H.A.S. wrote the paper with input from J.E.S, Z.G, and B.L.B.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2111060118/-/DCSupplemental.

Data Availability

The MATLAB codes for image processing and the estimation of surface tension and contact angle are shared on GitHub: https://github.com/JudyQYang/Bacterial_corner_flow_codes. The authors confirm that the data supporting the findings of this study can be extracted from the figures and movies of the article and its supporting information. All other study data are included in the article and/or supporting information.

  • Accepted July 29, 2021.

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Evidence for biosurfactant-induced flow in corners and bacterial spreading in unsaturated porous media - pnas.org
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