Mechanical stimuli activate gene expression via a cell envelope stress sensing pathway
Abstract Mechanosensitive mechanisms are often used to sense damage to tissue structure, stimulating matrix synthesis and repair. While this kind of mechanoregulatory process is well recognized in eukaryotic systems, it is not known whether such a process occurs in bacteria. In Vibrio cholerae, anti...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-08-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-40897-w |
| _version_ | 1797576832747307008 |
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| author | Christine E. Harper Wenyao Zhang Junsung Lee Jung-Ho Shin Megan R. Keller Ellen van Wijngaarden Emily Chou Zhaohong Wang Tobias Dörr Peng Chen Christopher J. Hernandez |
| author_facet | Christine E. Harper Wenyao Zhang Junsung Lee Jung-Ho Shin Megan R. Keller Ellen van Wijngaarden Emily Chou Zhaohong Wang Tobias Dörr Peng Chen Christopher J. Hernandez |
| author_sort | Christine E. Harper |
| collection | DOAJ |
| description | Abstract Mechanosensitive mechanisms are often used to sense damage to tissue structure, stimulating matrix synthesis and repair. While this kind of mechanoregulatory process is well recognized in eukaryotic systems, it is not known whether such a process occurs in bacteria. In Vibrio cholerae, antibiotic-induced damage to the load-bearing cell wall promotes increased signaling by the two-component system VxrAB, which stimulates cell wall synthesis. Here we show that changes in mechanical stress within the cell envelope are sufficient to stimulate VxrAB signaling in the absence of antibiotics. We applied mechanical forces to individual bacteria using three distinct loading modalities: extrusion loading within a microfluidic device, direct compression and hydrostatic pressure. In all cases, VxrAB signaling, as indicated by a fluorescent protein reporter, was increased in cells submitted to greater magnitudes of mechanical loading, hence diverse forms of mechanical stimuli activate VxrAB signaling. Reduction in cell envelope stiffness following removal of the endopeptidase ShyA led to large increases in cell envelope deformation and substantially increased VxrAB response, further supporting the responsiveness of VxrAB. Our findings demonstrate a mechanosensitive gene regulatory system in bacteria and suggest that mechanical signals may contribute to the regulation of cell wall homeostasis. |
| first_indexed | 2024-03-10T21:59:17Z |
| format | Article |
| id | doaj.art-55c378c485e9407bae72177b781bbc90 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-10T21:59:17Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-55c378c485e9407bae72177b781bbc902023-11-19T13:00:22ZengNature PortfolioScientific Reports2045-23222023-08-0113111210.1038/s41598-023-40897-wMechanical stimuli activate gene expression via a cell envelope stress sensing pathwayChristine E. Harper0Wenyao Zhang1Junsung Lee2Jung-Ho Shin3Megan R. Keller4Ellen van Wijngaarden5Emily Chou6Zhaohong Wang7Tobias Dörr8Peng Chen9Christopher J. Hernandez10Sibley School of Mechanical and Aerospace Engineering, Cornell UniversityDepartment of Chemistry and Chemical Biology, Cornell UniversitySibley School of Mechanical and Aerospace Engineering, Cornell UniversityWeill Institute for Cell and Molecular Biology, Cornell UniversityWeill Institute for Cell and Molecular Biology, Cornell UniversitySibley School of Mechanical and Aerospace Engineering, Cornell UniversitySibley School of Mechanical and Aerospace Engineering, Cornell UniversityDepartment of Chemistry and Chemical Biology, Cornell UniversityWeill Institute for Cell and Molecular Biology, Cornell UniversityDepartment of Chemistry and Chemical Biology, Cornell UniversityDepartment of Bioengineering and Therapeutic Sciences and Orthopaedic Surgery, University of CaliforniaAbstract Mechanosensitive mechanisms are often used to sense damage to tissue structure, stimulating matrix synthesis and repair. While this kind of mechanoregulatory process is well recognized in eukaryotic systems, it is not known whether such a process occurs in bacteria. In Vibrio cholerae, antibiotic-induced damage to the load-bearing cell wall promotes increased signaling by the two-component system VxrAB, which stimulates cell wall synthesis. Here we show that changes in mechanical stress within the cell envelope are sufficient to stimulate VxrAB signaling in the absence of antibiotics. We applied mechanical forces to individual bacteria using three distinct loading modalities: extrusion loading within a microfluidic device, direct compression and hydrostatic pressure. In all cases, VxrAB signaling, as indicated by a fluorescent protein reporter, was increased in cells submitted to greater magnitudes of mechanical loading, hence diverse forms of mechanical stimuli activate VxrAB signaling. Reduction in cell envelope stiffness following removal of the endopeptidase ShyA led to large increases in cell envelope deformation and substantially increased VxrAB response, further supporting the responsiveness of VxrAB. Our findings demonstrate a mechanosensitive gene regulatory system in bacteria and suggest that mechanical signals may contribute to the regulation of cell wall homeostasis.https://doi.org/10.1038/s41598-023-40897-w |
| spellingShingle | Christine E. Harper Wenyao Zhang Junsung Lee Jung-Ho Shin Megan R. Keller Ellen van Wijngaarden Emily Chou Zhaohong Wang Tobias Dörr Peng Chen Christopher J. Hernandez Mechanical stimuli activate gene expression via a cell envelope stress sensing pathway Scientific Reports |
| title | Mechanical stimuli activate gene expression via a cell envelope stress sensing pathway |
| title_full | Mechanical stimuli activate gene expression via a cell envelope stress sensing pathway |
| title_fullStr | Mechanical stimuli activate gene expression via a cell envelope stress sensing pathway |
| title_full_unstemmed | Mechanical stimuli activate gene expression via a cell envelope stress sensing pathway |
| title_short | Mechanical stimuli activate gene expression via a cell envelope stress sensing pathway |
| title_sort | mechanical stimuli activate gene expression via a cell envelope stress sensing pathway |
| url | https://doi.org/10.1038/s41598-023-40897-w |
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