Matrix-trapped viruses can prevent invasion of bacterial biofilms by colonizing cells

  1. Matthew C Bond
  2. Lucia Vidakovic
  3. Praveen K Singh
  4. Knut Drescher
  5. Carey D Nadell  Is a corresponding author
  1. Dartmouth, United States
  2. Max Planck Institute for Terrestrial Microbiology, Germany
  3. University of Basel, Switzerland

Abstract

Bacteriophages can be trapped in the matrix of bacterial biofilms, such that the cells inside them are protected. It is not known whether these phages are still infectious and whether they pose a threat to newly arriving bacteria. Here we address these questions using Escherichia coli and its lytic phage T7. Prior work has demonstrated that T7 phages are bound in the outermost curli polymer layers of the E. coli biofilm matrix. We show that these phages do remain viable and can kill colonizing cells that are T7-susceptible. If cells colonize a resident biofilm before phages do, we find that they can still be killed by phage exposure if it occurs soon thereafter. However, if colonizing cells are present on the biofilm long enough before phage exposure, they gain phage protection via envelopment within curli-producing clusters of the resident biofilm cells.

Data availability

Raw data for the entire study has been provided in the source data file with the re-submission

Article and author information

Author details

  1. Matthew C Bond

    Biological Sciences, Dartmouth, Hanover, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Lucia Vidakovic

    Systems and Synthetic Biology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5289-5163
  3. Praveen K Singh

    Systems and Synthetic Biology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0254-7400
  4. Knut Drescher

    University of Basel, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7340-2444
  5. Carey D Nadell

    Biological Sciences, Dartmouth, Hanover, United States
    For correspondence
    carey.d.nadell@dartmouth.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1751-4895

Funding

National Science Foundation (MCB 1817342)

  • Carey D Nadell

National Science Foundation (IOS 2017879)

  • Carey D Nadell

National Institutes of Health (P30-DK117469)

  • Carey D Nadell

National Institutes of Health (2R01AI081838)

  • Carey D Nadell

Cystic Fibrosis Foundation (STANTO15RO)

  • Carey D Nadell

National Institutes of Health (P20-GM113132)

  • Carey D Nadell

Human Frontier Science Program (RGY0077/2020)

  • Carey D Nadell

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

Reviewing Editor

  1. Wenying Shou, University College London, United Kingdom

Publication history

  1. Received: December 1, 2020
  2. Accepted: July 8, 2021
  3. Accepted Manuscript published: July 9, 2021 (version 1)
  4. Version of Record published: August 6, 2021 (version 2)

Copyright

© 2021, Bond 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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  1. Matthew C Bond
  2. Lucia Vidakovic
  3. Praveen K Singh
  4. Knut Drescher
  5. Carey D Nadell
(2021)
Matrix-trapped viruses can prevent invasion of bacterial biofilms by colonizing cells
eLife 10:e65355.
https://doi.org/10.7554/eLife.65355
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Further reading

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    Background: The variation in the pathogen type as well as the spatial heterogeneity of predictors make the generality of any associations with pathogen discovery debatable. Our previous work confirmed that the association of a group of predictors differed across different types of RNA viruses, yet there have been no previous comparisons of the specific predictors for RNA virus discovery in different regions. The aim of the current study was to close the gap by investigating whether predictors of discovery rates within three regions-the United States, China, and Africa-differ from one another and from those at the global level.

    Methods: Based on a comprehensive list of human-infective RNA viruses, we collated published data on first discovery of each species in each region. We used a Poisson boosted regression tree (BRT) model to examine the relationship between virus discovery and 33 predictors representing climate, socio-economics, land use, and biodiversity across each region separately. The discovery probability in three regions in 2010-2019 was mapped using the fitted models and historical predictors.

    Results: The numbers of human-infective virus species discovered in the United States, China, and Africa up to 2019 were 95, 80 and 107 respectively, with China lagging behind the other two regions. In each region, discoveries were clustered in hotspots. BRT modelling suggested that in all three regions RNA virus discovery was better predicted by land use and socio-economic variables than climatic variables and biodiversity, though the relative importance of these predictors varied by region. Map of virus discovery probability in 2010-2019 indicated several new hotspots outside historical high-risk areas. Most new virus species since 2010 in each region (6/6 in the United States, 19/19 in China, 12/19 in Africa) were discovered in high-risk areas as predicted by our model.

    Conclusions: The drivers of spatiotemporal variation in virus discovery rates vary in different regions of the world. Within regions virus discovery is driven mainly by land-use and socio-economic variables; climate and biodiversity variables are consistently less important predictors than at a global scale. Potential new discovery hotspots in 2010-2019 are identified. Results from the study could guide active surveillance for new human-infective viruses in local high-risk areas.

    Funding: FFZ is funded by the Darwin Trust of Edinburgh (https://darwintrust.bio.ed.ac.uk/). MEJW has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No. 874735 (VEO) (https://www.veo-europe.eu/).