The pH Robustness of Bacterial Sensing
ABSTRACT Bacteria have evolved many different signal transduction systems to sense and respond to changing environmental conditions. Signal integration is mainly achieved by signal recognition at extracytosolic ligand-binding domains (LBDs) of receptors. Hundreds of different LBDs have been reported...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-10-01
|
| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.01650-22 |
| _version_ | 1828163848610250752 |
|---|---|
| author | Elizabet Monteagudo-Cascales David Martín-Mora Wenhao Xu Victor Sourjik Miguel A. Matilla Álvaro Ortega Tino Krell |
| author_facet | Elizabet Monteagudo-Cascales David Martín-Mora Wenhao Xu Victor Sourjik Miguel A. Matilla Álvaro Ortega Tino Krell |
| author_sort | Elizabet Monteagudo-Cascales |
| collection | DOAJ |
| description | ABSTRACT Bacteria have evolved many different signal transduction systems to sense and respond to changing environmental conditions. Signal integration is mainly achieved by signal recognition at extracytosolic ligand-binding domains (LBDs) of receptors. Hundreds of different LBDs have been reported, and our understanding of their sensing properties is growing. Receptors must function over a range of environmental pH values, but there is little information available on the robustness of sensing as a function of pH. Here, we have used isothermal titration calorimetry to determine the pH dependence of ligand recognition by nine LBDs that cover all major LBD superfamilies, of periplasmic solute-binding proteins, and cytosolic LBDs. We show that periplasmic LBDs recognize ligands over a very broad pH range, frequently stretching over eight pH units. This wide pH range contrasts with a much narrower pH response range of the cytosolic LBDs analyzed. Many LBDs must be dimeric to bind ligands, and analytical ultracentrifugation studies showed that the LBD of the Tar chemoreceptor forms dimers over the entire pH range tested. The pH dependences of Pseudomonas aeruginosa motility and chemotaxis were bell-shaped and centered at pH 7.0. Evidence for pH robustness of signaling in vivo was obtained by Förster Resonance Energy Transfer (FRET) measurements of the chemotaxis pathway responses in Escherichia coli. Bacteria have evolved several strategies to cope with extreme pH, such as periplasmic chaperones for protein refolding. The intrinsic pH resistance of periplasmic LBDs appears to be another strategy that permits bacteria to survive under adverse conditions. IMPORTANCE Demonstration of the pH robustness of extracytoplasmic sensing reveals a previously undescribed evolutionary mechanism that enables bacteria to monitor environmental changes under changing conditions. This mechanism includes the maintenance of the dimeric state of four-helixbundle ligand-binding domains (LBDs). The construction of biosensors is a rapidly growing field of research, and their use to monitor the progression of the COVID-19 pandemic has impressively demonstrated their usefulness. LBDs represent an enormous reservoir of binding modules that can be used to create novel biosensors. Among ligands recognized by LBDs are neurotransmitters, hormones, and quorum-sensing signals. The demonstration that extracytosolic LBDs bind their signals over a wide range of pH values will facilitate the design of biosensors that function under highly variable conditions of acidity and alkalinity. |
| first_indexed | 2024-04-12T01:15:36Z |
| format | Article |
| id | doaj.art-a228c2f63cd243179bd7a8a7c04905cd |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-04-12T01:15:36Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-a228c2f63cd243179bd7a8a7c04905cd2022-12-22T03:53:59ZengAmerican Society for MicrobiologymBio2150-75112022-10-0113510.1128/mbio.01650-22The pH Robustness of Bacterial SensingElizabet Monteagudo-Cascales0David Martín-Mora1Wenhao Xu2Victor Sourjik3Miguel A. Matilla4Álvaro Ortega5Tino Krell6Department of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainDepartment of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainMax Planck Institute for Terrestrial Microbiology and Center for Synthetic Microbiology (SYNMIKRO), Marburg, GermanyMax Planck Institute for Terrestrial Microbiology and Center for Synthetic Microbiology (SYNMIKRO), Marburg, GermanyDepartment of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainDepartment of Biochemistry and Molecular Biology ‘B’ and Immunology, Faculty of Chemistry, University of Murcia, Regional Campus of International Excellence “Campus Mare Nostrum”, Murcia, SpainDepartment of Environmental Protection, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Granada, SpainABSTRACT Bacteria have evolved many different signal transduction systems to sense and respond to changing environmental conditions. Signal integration is mainly achieved by signal recognition at extracytosolic ligand-binding domains (LBDs) of receptors. Hundreds of different LBDs have been reported, and our understanding of their sensing properties is growing. Receptors must function over a range of environmental pH values, but there is little information available on the robustness of sensing as a function of pH. Here, we have used isothermal titration calorimetry to determine the pH dependence of ligand recognition by nine LBDs that cover all major LBD superfamilies, of periplasmic solute-binding proteins, and cytosolic LBDs. We show that periplasmic LBDs recognize ligands over a very broad pH range, frequently stretching over eight pH units. This wide pH range contrasts with a much narrower pH response range of the cytosolic LBDs analyzed. Many LBDs must be dimeric to bind ligands, and analytical ultracentrifugation studies showed that the LBD of the Tar chemoreceptor forms dimers over the entire pH range tested. The pH dependences of Pseudomonas aeruginosa motility and chemotaxis were bell-shaped and centered at pH 7.0. Evidence for pH robustness of signaling in vivo was obtained by Förster Resonance Energy Transfer (FRET) measurements of the chemotaxis pathway responses in Escherichia coli. Bacteria have evolved several strategies to cope with extreme pH, such as periplasmic chaperones for protein refolding. The intrinsic pH resistance of periplasmic LBDs appears to be another strategy that permits bacteria to survive under adverse conditions. IMPORTANCE Demonstration of the pH robustness of extracytoplasmic sensing reveals a previously undescribed evolutionary mechanism that enables bacteria to monitor environmental changes under changing conditions. This mechanism includes the maintenance of the dimeric state of four-helixbundle ligand-binding domains (LBDs). The construction of biosensors is a rapidly growing field of research, and their use to monitor the progression of the COVID-19 pandemic has impressively demonstrated their usefulness. LBDs represent an enormous reservoir of binding modules that can be used to create novel biosensors. Among ligands recognized by LBDs are neurotransmitters, hormones, and quorum-sensing signals. The demonstration that extracytosolic LBDs bind their signals over a wide range of pH values will facilitate the design of biosensors that function under highly variable conditions of acidity and alkalinity.https://journals.asm.org/doi/10.1128/mbio.01650-22signal transductionreceptorssensor domainspH robustnessbacterial adaptationpH |
| spellingShingle | Elizabet Monteagudo-Cascales David Martín-Mora Wenhao Xu Victor Sourjik Miguel A. Matilla Álvaro Ortega Tino Krell The pH Robustness of Bacterial Sensing mBio signal transduction receptors sensor domains pH robustness bacterial adaptation pH |
| title | The pH Robustness of Bacterial Sensing |
| title_full | The pH Robustness of Bacterial Sensing |
| title_fullStr | The pH Robustness of Bacterial Sensing |
| title_full_unstemmed | The pH Robustness of Bacterial Sensing |
| title_short | The pH Robustness of Bacterial Sensing |
| title_sort | ph robustness of bacterial sensing |
| topic | signal transduction receptors sensor domains pH robustness bacterial adaptation pH |
| url | https://journals.asm.org/doi/10.1128/mbio.01650-22 |
| work_keys_str_mv | AT elizabetmonteagudocascales thephrobustnessofbacterialsensing AT davidmartinmora thephrobustnessofbacterialsensing AT wenhaoxu thephrobustnessofbacterialsensing AT victorsourjik thephrobustnessofbacterialsensing AT miguelamatilla thephrobustnessofbacterialsensing AT alvaroortega thephrobustnessofbacterialsensing AT tinokrell thephrobustnessofbacterialsensing AT elizabetmonteagudocascales phrobustnessofbacterialsensing AT davidmartinmora phrobustnessofbacterialsensing AT wenhaoxu phrobustnessofbacterialsensing AT victorsourjik phrobustnessofbacterialsensing AT miguelamatilla phrobustnessofbacterialsensing AT alvaroortega phrobustnessofbacterialsensing AT tinokrell phrobustnessofbacterialsensing |