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Cited by 171Bacteriophages and microbial interactionsBacterial Genetics and BiotechnologyEvolution and Genetic Dynamics

High-throughput mapping of the phage resistance landscape in E. coli

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Mutalik, Vivek K., Adler, Benjamin A., Rishi, Harneet S., Piya, Denish, Zhong, Crystal, Koskella, Britt, Kutter, Elizabeth M., Calendar, Richard +4 more·2020·PLOS Biology
DOI 10.1371/journal.pbio.3000877PMC PMC7553319

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Abstract

Bacteriophages (phages) are critical players in the dynamics and function of microbial communities and drive processes as diverse as global biogeochemical cycles and human health. Phages tend to be predators finely tuned to attack specific hosts, even down to the strain level, which in turn defend themselves using an array of mechanisms. However, to date, efforts to rapidly and comprehensively identify bacterial host factors important in phage infection and resistance have yet to be fully realized. Here, we globally map the host genetic determinants involved in resistance to 14 phylogenetically diverse double-stranded DNA phages using two model Escherichia coli strains (K-12 and BL21) with known sequence divergence to demonstrate strain-specific differences. Using genome-wide loss-of-function and gain-of-function genetic technologies, we are able to confirm previously described phage receptors as well as uncover a number of previously unknown host factors that confer resistance to one or more of these phages. We uncover differences in resistance factors that strongly align with the susceptibility of K-12 and BL21 to specific phage. We also identify both phage-specific mechanisms, such as the unexpected role of cyclic-di-GMP in host sensitivity to phage N4, and more generic defenses, such as the overproduction of colanic acid capsular polysaccharide that defends against a wide array of phages. Our results indicate that host responses to phages can occur via diverse cellular mechanisms. Our systematic and high-throughput genetic workflow to characterize phage-host interaction determinants can be extended to diverse bacteria to generate datasets that allow predictive models of how phage-mediated selection will shape bacterial phenotype and evolution. The results of this study and future efforts to map the phage resistance landscape will lead to new insights into the coevolution of hosts and their phage, which can ultimately be used to design better phage therapeutic treatments and tools for precision microbiome engineering.

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Authors
Mutalik, V. K., Adler, B. A., Rishi, H. S., Piya, D., Zhong, C., Koskella, B., Kutter, E. M., Calendar, R., Novichkov, P. S., Price, M. N., Deutschbauer, A. M., & Arkin, A. P.
Affiliations
  • Lawrence Berkeley National Laboratory (US)
  • Innovative Genomics Institute (US)
  • University of California, Berkeley (US)
  • The Evergreen State College (US)
Corresponding author
  • Mutalik, Vivek K.
  • Arkin, Adam P.
ORCID
Venue
PLOS Biology
Publisher
Public Library of Science (PLoS)
Published
2020-10-13
Volume
18
Issue
10
Pages
e3000877
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.3000877
PMC
PMC7553319
OpenAlex
W3092072294
Cited by
171
References
7
Citations by year
2026: 23 · 2025: 36 · 2024: 29 · 2023: 32 · 2022: 22 · 2021: 22 · 2020: 7
FWCI
11.02
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
Funders
  • Innovative Genomics Institute
  • U.S. Department of Energy (DE-AC02-05CH11231)
Topics
  • Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
phage resistance, phage-host interactions, Escherichia coli, phage receptor, host defense, c-di-GMP, colanic acid, capsular polysaccharide, strain-specific resistance, phage therapy
MeSH terms
Bacterial Proteins, Bacteriophages, DNA, Escherichia coli, Cyclic GMP, Mutation, Phenotype, Suppression, Genetic, Reproducibility of Results, Down-Regulation, Gene Expression Regulation, Bacterial, Genome, Bacterial, Genes, Essential, Biosynthetic Pathways, CRISPR-Cas Systems

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