Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming.
The two-component signalling system (TCS) comprising a histidine kinase (HK) and a response regulator (RR) is the predominant bacterial sense-and-response machinery. Because bacterial cells usually encode a number of TCSs to adapt to various ecological niches, the specificity of a TCS is in the cent...
| Main Authors: | , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-08-01
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| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.1007952 |
| _version_ | 1818582393572818944 |
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| author | Shou-Ting Cheng Fang-Fang Wang Wei Qian |
| author_facet | Shou-Ting Cheng Fang-Fang Wang Wei Qian |
| author_sort | Shou-Ting Cheng |
| collection | DOAJ |
| description | The two-component signalling system (TCS) comprising a histidine kinase (HK) and a response regulator (RR) is the predominant bacterial sense-and-response machinery. Because bacterial cells usually encode a number of TCSs to adapt to various ecological niches, the specificity of a TCS is in the centre of regulation. Specificity of TCS is defined by the capability and velocity of phosphoryl transfer between a cognate HK and a RR. Here, we provide genetic, enzymology and structural data demonstrating that the second messenger cyclic-di-GMP physically and specifically binds to RavS, a HK of the phytopathogenic, gram-negative bacterium Xanthomonas campestris pv. campestris. The [c-di-GMP]-RavS interaction substantially promotes specificity between RavS and RavR, a GGDEF-EAL domain-containing RR, by reinforcing the kinetic preference of RavS to phosphorylate RavR. [c-di-GMP]-RavS binding effectively decreases the phosphorylation level of RavS and negatively regulates bacterial swimming. Intriguingly, the EAL domain of RavR counteracts the above regulation by degrading c-di-GMP and then increasing the level of phosphorylated RavS. Therefore, RavR acts as a bifunctional phosphate sink that finely controls the level of phosphorylated RavS. These biochemical processes interactively modulate the phosphoryl flux between RavS-RavR and bacterial lifestyle transition. Our results revealed that c-di-GMP acts as an allosteric effector to dynamically modulate specificity between HK and RR. |
| first_indexed | 2024-12-16T07:48:41Z |
| format | Article |
| id | doaj.art-4e61c68159f3489185623cf93ff950b5 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-12-16T07:48:41Z |
| publishDate | 2019-08-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-4e61c68159f3489185623cf93ff950b52022-12-21T22:38:55ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742019-08-01158e100795210.1371/journal.ppat.1007952Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming.Shou-Ting ChengFang-Fang WangWei QianThe two-component signalling system (TCS) comprising a histidine kinase (HK) and a response regulator (RR) is the predominant bacterial sense-and-response machinery. Because bacterial cells usually encode a number of TCSs to adapt to various ecological niches, the specificity of a TCS is in the centre of regulation. Specificity of TCS is defined by the capability and velocity of phosphoryl transfer between a cognate HK and a RR. Here, we provide genetic, enzymology and structural data demonstrating that the second messenger cyclic-di-GMP physically and specifically binds to RavS, a HK of the phytopathogenic, gram-negative bacterium Xanthomonas campestris pv. campestris. The [c-di-GMP]-RavS interaction substantially promotes specificity between RavS and RavR, a GGDEF-EAL domain-containing RR, by reinforcing the kinetic preference of RavS to phosphorylate RavR. [c-di-GMP]-RavS binding effectively decreases the phosphorylation level of RavS and negatively regulates bacterial swimming. Intriguingly, the EAL domain of RavR counteracts the above regulation by degrading c-di-GMP and then increasing the level of phosphorylated RavS. Therefore, RavR acts as a bifunctional phosphate sink that finely controls the level of phosphorylated RavS. These biochemical processes interactively modulate the phosphoryl flux between RavS-RavR and bacterial lifestyle transition. Our results revealed that c-di-GMP acts as an allosteric effector to dynamically modulate specificity between HK and RR.https://doi.org/10.1371/journal.ppat.1007952 |
| spellingShingle | Shou-Ting Cheng Fang-Fang Wang Wei Qian Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming. PLoS Pathogens |
| title | Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming. |
| title_full | Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming. |
| title_fullStr | Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming. |
| title_full_unstemmed | Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming. |
| title_short | Cyclic-di-GMP binds to histidine kinase RavS to control RavS-RavR phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming. |
| title_sort | cyclic di gmp binds to histidine kinase ravs to control ravs ravr phosphotransfer and regulates the bacterial lifestyle transition between virulence and swimming |
| url | https://doi.org/10.1371/journal.ppat.1007952 |
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