Mechanosensation induces persistent bacterial growth during bacteriophage predation
ABSTRACTAlthough the relationship between bacteria and lytic bacteriophage is fundamentally antagonistic, these microbes not only coexist but thrive side by side in myriad ecological environments. The mechanisms by which coexistence is achieved, however, are not fully understood. By examining Escher...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.02766-22 |
| _version_ | 1797378896179494912 |
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| author | Guy Mason Matthew J. Footer Enrique R. Rojas |
| author_facet | Guy Mason Matthew J. Footer Enrique R. Rojas |
| author_sort | Guy Mason |
| collection | DOAJ |
| description | ABSTRACTAlthough the relationship between bacteria and lytic bacteriophage is fundamentally antagonistic, these microbes not only coexist but thrive side by side in myriad ecological environments. The mechanisms by which coexistence is achieved, however, are not fully understood. By examining Escherichia coli and bacteriophage T7 population dynamics at the single-cell and single-virion level using a novel microfluidics assay, we observed bacteria growing “persistently” when perfused with high-titer bacteriophage. Bacteriophage persistence occurred at a frequency five orders of magnitude higher than is expected from the natural selection of bacteriophage-resistant mutants. Rather, the frequency of persistence was correlated with the degree to which the bacteria were mechanically compressed by the microfluidic perfusion chamber. Using a combination of mutagenesis and fluorescent imaging techniques, we discovered that compression induces persistence by activating the Rcs phosphorelay pathway, which results in the synthesis of extracellular capsule that sterically blocks bacteriophage adsorption. Other forms of mechanical perturbation also promoted Rcs activity and persistence. These findings have important implications for our understanding of microbial ecology in many important environments, including the gut and the soil, where bacteria grow in confinement.IMPORTANCEBacteria and bacteriophage form one of the most important predator-prey relationships on earth, yet how the long-term stability of this ecological interaction is achieved is unclear. Here, we demonstrate that Escherichia coli can rapidly grow during bacteriophage predation if they are doing so in spatially confined environments. This discovery revises our understanding of bacteria-bacteriophage population dynamics in many real-world environments where bacteria grow in confinement, such as the gut and the soil. Additionally, this result has clear implications for the potential of bacteriophage therapy and the role of mechanosensation during bacterial pathogenesis. |
| first_indexed | 2024-03-08T20:14:15Z |
| format | Article |
| id | doaj.art-9ab4c713e52741f987612384e5fd2e77 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-03-08T20:14:15Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-9ab4c713e52741f987612384e5fd2e772023-12-22T19:53:44ZengAmerican Society for MicrobiologymBio2150-75112023-12-0114610.1128/mbio.02766-22Mechanosensation induces persistent bacterial growth during bacteriophage predationGuy Mason0Matthew J. Footer1Enrique R. Rojas2Department of Biology, Center for Genomics and Systems Biology, New York University, New York, New York, USADepartment of Biology, Howard Hughes Medical Institute, University of Washington, Seattle, Washington, USADepartment of Biology, Center for Genomics and Systems Biology, New York University, New York, New York, USAABSTRACTAlthough the relationship between bacteria and lytic bacteriophage is fundamentally antagonistic, these microbes not only coexist but thrive side by side in myriad ecological environments. The mechanisms by which coexistence is achieved, however, are not fully understood. By examining Escherichia coli and bacteriophage T7 population dynamics at the single-cell and single-virion level using a novel microfluidics assay, we observed bacteria growing “persistently” when perfused with high-titer bacteriophage. Bacteriophage persistence occurred at a frequency five orders of magnitude higher than is expected from the natural selection of bacteriophage-resistant mutants. Rather, the frequency of persistence was correlated with the degree to which the bacteria were mechanically compressed by the microfluidic perfusion chamber. Using a combination of mutagenesis and fluorescent imaging techniques, we discovered that compression induces persistence by activating the Rcs phosphorelay pathway, which results in the synthesis of extracellular capsule that sterically blocks bacteriophage adsorption. Other forms of mechanical perturbation also promoted Rcs activity and persistence. These findings have important implications for our understanding of microbial ecology in many important environments, including the gut and the soil, where bacteria grow in confinement.IMPORTANCEBacteria and bacteriophage form one of the most important predator-prey relationships on earth, yet how the long-term stability of this ecological interaction is achieved is unclear. Here, we demonstrate that Escherichia coli can rapidly grow during bacteriophage predation if they are doing so in spatially confined environments. This discovery revises our understanding of bacteria-bacteriophage population dynamics in many real-world environments where bacteria grow in confinement, such as the gut and the soil. Additionally, this result has clear implications for the potential of bacteriophage therapy and the role of mechanosensation during bacterial pathogenesis.https://journals.asm.org/doi/10.1128/mbio.02766-22cell mechanicsmicrobial ecologybacteriophage T7microfluidicsRcs pathway |
| spellingShingle | Guy Mason Matthew J. Footer Enrique R. Rojas Mechanosensation induces persistent bacterial growth during bacteriophage predation mBio cell mechanics microbial ecology bacteriophage T7 microfluidics Rcs pathway |
| title | Mechanosensation induces persistent bacterial growth during bacteriophage predation |
| title_full | Mechanosensation induces persistent bacterial growth during bacteriophage predation |
| title_fullStr | Mechanosensation induces persistent bacterial growth during bacteriophage predation |
| title_full_unstemmed | Mechanosensation induces persistent bacterial growth during bacteriophage predation |
| title_short | Mechanosensation induces persistent bacterial growth during bacteriophage predation |
| title_sort | mechanosensation induces persistent bacterial growth during bacteriophage predation |
| topic | cell mechanics microbial ecology bacteriophage T7 microfluidics Rcs pathway |
| url | https://journals.asm.org/doi/10.1128/mbio.02766-22 |
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