1. Microbiology and Infectious Disease
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Biofilms deform soft surfaces and disrupt epithelia

  1. Alice Cont
  2. Tamara Rossy
  3. Zainebe Al-Mayyah
  4. Alexandre Persat  Is a corresponding author
  1. Ecole Polytechnique Fédérale de Lausanne, Switzerland
Research Article
  • Cited 6
  • Views 2,243
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Cite this article as: eLife 2020;9:e56533 doi: 10.7554/eLife.56533

Abstract

During chronic infections and in microbiota, bacteria predominantly colonize their hosts as multicellular structures called biofilms. A common assumption is that biofilms exclusively interact with their hosts biochemically. However, the contributions of mechanics, while being central to the process of biofilm formation, have been overlooked as a factor influencing host physiology. Specifically, how biofilms form on soft, tissue-like materials remains unknown. Here we show that biofilms of the pathogens Vibrio cholerae and Pseudomonas aeruginosa can induce large deformations of soft synthetic hydrogels. Biofilms buildup internal mechanical stress as single cells grow within the elastic matrix. By combining mechanical measurements and mutations in matrix components, we found that biofilms deform by buckling, and that adhesion transmits these forces to their substrates. Finally, we demonstrate that V. cholerae biofilms can generate sufficient mechanical stress to deform and even disrupt soft epithelial cell monolayers, suggesting a mechanical mode of infection.

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Article and author information

Author details

  1. Alice Cont

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Tamara Rossy

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Zainebe Al-Mayyah

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Alexandre Persat

    Institute for Bioengineering and Global Health Institute, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    For correspondence
    alexandre.persat@epfl.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8426-8255

Funding

Swiss National Science Foundation

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

Cavaglieri Foundation

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

Fondation Beytout

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

Gebert Rüf Stiftung

  • Alice Cont
  • Tamara Rossy
  • Zainebe Al-Mayyah
  • Alexandre Persat

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Petra Anne Levin, Washington University in St. Louis, United States

Publication history

  1. Received: March 2, 2020
  2. Accepted: August 23, 2020
  3. Accepted Manuscript published: October 7, 2020 (version 1)
  4. Version of Record published: October 14, 2020 (version 2)

Copyright

© 2020, Cont et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

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    East Asians (EAs) experience worse metabolic health outcomes compared to other ethnic groups at lower body mass indices; however, the potential role of the gut microbiota in contributing to these health disparities remains unknown. We conducted a multi-omic study of 46 lean and obese East Asian and White participants living in the San Francisco Bay Area, revealing marked differences between ethnic groups in bacterial richness and community structure. White individuals were enriched for the mucin-degrading Akkermansia muciniphila. East Asian subjects had increased levels of multiple bacterial phyla, fermentative pathways detected by metagenomics, and the short-chain fatty acid end-products acetate, propionate, and isobutyrate. Differences in the gut microbiota between the East Asian and White subjects could not be explained by dietary intake, were more pronounced in lean individuals, and were associated with current geographical location. Microbiome transplantations into germ-free mice demonstrated stable diet- and host genotype-independent differences between the gut microbiotas of East Asian and White individuals that differentially impact host body composition. Taken together, our findings add to the growing body of literature describing microbiome variations between ethnicities and provide a starting point for defining the mechanisms through which the microbiome may shape disparate health outcomes in East Asians.

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    For many intracellular pathogens, the phagosome is the site of events and interactions that shape infection outcome. Phagosomal membrane damage, in particular, is proposed to benefit invading pathogens. To define the innate immune consequences of this damage, we profiled macrophage transcriptional responses to wild-type Mycobacterium tuberculosis (Mtb) and mutants that fail to damage the phagosomal membrane. We identified a set of genes with enhanced expression in response to the mutants. These genes represented a late component of the TLR2-dependent transcriptional response to Mtb, distinct from an earlier component that included Tnf. Expression of the later component was inherent to TLR2 activation, dependent upon endosomal uptake, and enhanced by phagosome acidification. Canonical Mtb virulence factors that contribute to phagosomal membrane damage blunted phagosome acidification and undermined the endosome-specific response. Profiling cell survival and bacterial growth in macrophages demonstrated that the attenuation of these mutants is partially dependent upon TLR2. Further, TLR2 contributed to the attenuated phenotype of one of these mutants in a murine model of infection. These results demonstrate two distinct components of the TLR2 response and identify a component dependent upon endosomal uptake as a point where pathogenic bacteria interfere with the generation of effective inflammation. This interference promotes tuberculosis (TB) pathogenesis in both macrophage and murine infection models.