Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP
Stable surface adhesion of cells is one of the early pivotal steps in bacterial biofilm formation, a prevalent adaptation strategy in response to changing environments. In Pseudomonas fluorescens, this process is regulated by the Lap system and the second messenger cyclic-di-GMP. High cytoplasmic le...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2014-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/03650 |
| _version_ | 1828221893374640128 |
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| author | Debashree Chatterjee Richard B Cooley Chelsea D Boyd Ryan A Mehl George A O'Toole Holger Sondermann |
| author_facet | Debashree Chatterjee Richard B Cooley Chelsea D Boyd Ryan A Mehl George A O'Toole Holger Sondermann |
| author_sort | Debashree Chatterjee |
| collection | DOAJ |
| description | Stable surface adhesion of cells is one of the early pivotal steps in bacterial biofilm formation, a prevalent adaptation strategy in response to changing environments. In Pseudomonas fluorescens, this process is regulated by the Lap system and the second messenger cyclic-di-GMP. High cytoplasmic levels of cyclic-di-GMP activate the transmembrane receptor LapD that in turn recruits the periplasmic protease LapG, preventing it from cleaving a cell surface-bound adhesin, thereby promoting cell adhesion. In this study, we elucidate the molecular basis of LapG regulation by LapD and reveal a remarkably sensitive switching mechanism that is controlled by LapD's HAMP domain. LapD appears to act as a coincidence detector, whereby a weak interaction of LapG with LapD transmits a transient outside-in signal that is reinforced only when cyclic-di-GMP levels increase. Given the conservation of key elements of this receptor system in many bacterial species, the results are broadly relevant for cyclic-di-GMP- and HAMP domain-regulated transmembrane signaling. |
| first_indexed | 2024-04-12T16:46:46Z |
| format | Article |
| id | doaj.art-1a908a9476a04e1f807be5dd4f8753cb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:46:46Z |
| publishDate | 2014-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-1a908a9476a04e1f807be5dd4f8753cb2022-12-22T03:24:32ZengeLife Sciences Publications LtdeLife2050-084X2014-09-01310.7554/eLife.03650Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMPDebashree Chatterjee0Richard B Cooley1Chelsea D Boyd2Ryan A Mehl3George A O'Toole4Holger Sondermann5Department of Molecular Medicine, College of Veterinary Medicine, Cornell University, Ithaca, United StatesDepartment of Molecular Medicine, College of Veterinary Medicine, Cornell University, Ithaca, United StatesDepartment of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, United StatesDepartment of Biochemistry and Biophysics, Oregon State University, Corvallis, United StatesDepartment of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, United StatesDepartment of Molecular Medicine, College of Veterinary Medicine, Cornell University, Ithaca, United StatesStable surface adhesion of cells is one of the early pivotal steps in bacterial biofilm formation, a prevalent adaptation strategy in response to changing environments. In Pseudomonas fluorescens, this process is regulated by the Lap system and the second messenger cyclic-di-GMP. High cytoplasmic levels of cyclic-di-GMP activate the transmembrane receptor LapD that in turn recruits the periplasmic protease LapG, preventing it from cleaving a cell surface-bound adhesin, thereby promoting cell adhesion. In this study, we elucidate the molecular basis of LapG regulation by LapD and reveal a remarkably sensitive switching mechanism that is controlled by LapD's HAMP domain. LapD appears to act as a coincidence detector, whereby a weak interaction of LapG with LapD transmits a transient outside-in signal that is reinforced only when cyclic-di-GMP levels increase. Given the conservation of key elements of this receptor system in many bacterial species, the results are broadly relevant for cyclic-di-GMP- and HAMP domain-regulated transmembrane signaling.https://elifesciences.org/articles/03650biofilm formationsignalingc-di-GMPcell adhesiontransmembrane proteinbacterial pathogen |
| spellingShingle | Debashree Chatterjee Richard B Cooley Chelsea D Boyd Ryan A Mehl George A O'Toole Holger Sondermann Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP eLife biofilm formation signaling c-di-GMP cell adhesion transmembrane protein bacterial pathogen |
| title | Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP |
| title_full | Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP |
| title_fullStr | Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP |
| title_full_unstemmed | Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP |
| title_short | Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-di-GMP |
| title_sort | mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic di gmp |
| topic | biofilm formation signaling c-di-GMP cell adhesion transmembrane protein bacterial pathogen |
| url | https://elifesciences.org/articles/03650 |
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