Cross-talk between bacterial two-component systems drives stepwise regulation of flagellar biosynthesis in swarming development
Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component system (TCS), which typically comprises a sensor kinase and a specific cognate response regulator, to properly react to environmental changes. We...
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Published in | Biochemical and biophysical research communications Vol. 489; no. 1; pp. 70 - 75 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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15.07.2017
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Abstract | Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component system (TCS), which typically comprises a sensor kinase and a specific cognate response regulator, to properly react to environmental changes. We previously showed that the TCS RssAB suppresses flagellar biosynthesis master regulator flhDC specifically in swarming lag phase to control surface migration timing without affecting expansion rate in Serratia marcescens swarming development. Here we demonstrate that the TCS QseBC, which has been found in several human pathogens involved in flagellar and virulence regulation, has cross-talk with RssAB. We demonstrate that the phosphorylated QseB repressed flhDC expression, reducing swarming migration rate with modest effect on migration initiation. Unexpectedly, the QseC can dephosphorylate non-cognate response regulator RssB. Deletion of qseC prolonged RssAB signaling, reduced flhDC expression, and delayed migration initiation. Our data suggest that QseC is a flagellar biosynthesis activator by de-repressing RssB ∼ P and QseB ∼ P respectively in lag and migration phases in a stage-specific manner in swarming development.
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•QseB regulates swarming migration rate and flagellar biosynthesis in S. marcescens.•Phosphorylation of QseB is required for its binding to flhDC promoter.•QseC dephosphorylates RssB and deactivates RssAB signaling in swarming lag. |
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AbstractList | Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component system (TCS), which typically comprises a sensor kinase and a specific cognate response regulator, to properly react to environmental changes. We previously showed that the TCS RssAB suppresses flagellar biosynthesis master regulator flhDC specifically in swarming lag phase to control surface migration timing without affecting expansion rate in Serratia marcescens swarming development. Here we demonstrate that the TCS QseBC, which has been found in several human pathogens involved in flagellar and virulence regulation, has cross-talk with RssAB. We demonstrate that the phosphorylated QseB repressed flhDC expression, reducing swarming migration rate with modest effect on migration initiation. Unexpectedly, the QseC can dephosphorylate non-cognate response regulator RssB. Deletion of qseC prolonged RssAB signaling, reduced flhDC expression, and delayed migration initiation. Our data suggest that QseC is a flagellar biosynthesis activator by de-repressing RssB ∼ P and QseB ∼ P respectively in lag and migration phases in a stage-specific manner in swarming development.Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component system (TCS), which typically comprises a sensor kinase and a specific cognate response regulator, to properly react to environmental changes. We previously showed that the TCS RssAB suppresses flagellar biosynthesis master regulator flhDC specifically in swarming lag phase to control surface migration timing without affecting expansion rate in Serratia marcescens swarming development. Here we demonstrate that the TCS QseBC, which has been found in several human pathogens involved in flagellar and virulence regulation, has cross-talk with RssAB. We demonstrate that the phosphorylated QseB repressed flhDC expression, reducing swarming migration rate with modest effect on migration initiation. Unexpectedly, the QseC can dephosphorylate non-cognate response regulator RssB. Deletion of qseC prolonged RssAB signaling, reduced flhDC expression, and delayed migration initiation. Our data suggest that QseC is a flagellar biosynthesis activator by de-repressing RssB ∼ P and QseB ∼ P respectively in lag and migration phases in a stage-specific manner in swarming development. Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component system (TCS), which typically comprises a sensor kinase and a specific cognate response regulator, to properly react to environmental changes. We previously showed that the TCS RssAB suppresses flagellar biosynthesis master regulator flhDC specifically in swarming lag phase to control surface migration timing without affecting expansion rate in Serratia marcescens swarming development. Here we demonstrate that the TCS QseBC, which has been found in several human pathogens involved in flagellar and virulence regulation, has cross-talk with RssAB. We demonstrate that the phosphorylated QseB repressed flhDC expression, reducing swarming migration rate with modest effect on migration initiation. Unexpectedly, the QseC can dephosphorylate non-cognate response regulator RssB. Deletion of qseC prolonged RssAB signaling, reduced flhDC expression, and delayed migration initiation. Our data suggest that QseC is a flagellar biosynthesis activator by de-repressing RssB ∼ P and QseB ∼ P respectively in lag and migration phases in a stage-specific manner in swarming development. [Display omitted] •QseB regulates swarming migration rate and flagellar biosynthesis in S. marcescens.•Phosphorylation of QseB is required for its binding to flhDC promoter.•QseC dephosphorylates RssB and deactivates RssAB signaling in swarming lag. Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component system (TCS), which typically comprises a sensor kinase and a specific cognate response regulator, to properly react to environmental changes. We previously showed that the TCS RssAB suppresses flagellar biosynthesis master regulator flhDC specifically in swarming lag phase to control surface migration timing without affecting expansion rate in Serratia marcescens swarming development. Here we demonstrate that the TCS QseBC, which has been found in several human pathogens involved in flagellar and virulence regulation, has cross-talk with RssAB. We demonstrate that the phosphorylated QseB repressed flhDC expression, reducing swarming migration rate with modest effect on migration initiation. Unexpectedly, the QseC can dephosphorylate non-cognate response regulator RssB. Deletion of qseC prolonged RssAB signaling, reduced flhDC expression, and delayed migration initiation. Our data suggest that QseC is a flagellar biosynthesis activator by de-repressing RssB ∼ P and QseB ∼ P respectively in lag and migration phases in a stage-specific manner in swarming development. Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component system (TCS), which typically comprises a sensor kinase and a specific cognate response regulator, to properly react to environmental changes. We previously showed that the TCS RssAB suppresses flagellar biosynthesis master regulator flhDC specifically in swarming lag phase to control surface migration timing without affecting expansion rate in Serratia marcescens swarming development. Here we demonstrate that the TCS QseBC, which has been found in several human pathogens involved in flagellar and virulence regulation, has cross-talk with RssAB. We demonstrate that the phosphorylated QseB repressed flhDC expression, reducing swarming migration rate with modest effect on migration initiation. Unexpectedly, the QseC can dephosphorylate non-cognate response regulator RssB. Deletion of qseC prolonged RssAB signaling, reduced flhDC expression, and delayed migration initiation. Our data suggest that QseC is a flagellar biosynthesis activator by de-repressing RssB ∼ P and QseB ∼ P respectively in lag and migration phases in a stage-specific manner in swarming development. |
Author | Lin, Chuan-Sheng Lai, Hsin-Chih Lu, Chia-Chen Huang, Hsiou-Chen Chang, Chih-Jung Tsai, Sheng-Hui Tsai, Yu-Huan Wei, Chia-Fong |
Author_xml | – sequence: 1 givenname: Chia-Fong surname: Wei fullname: Wei, Chia-Fong organization: Department of Medical Biotechnology and Laboratory Science, Center for Molecular and Clinical Immunology, College of Medicine, Chang Gung University, Taoyuan, Taiwan – sequence: 2 givenname: Yu-Huan surname: Tsai fullname: Tsai, Yu-Huan organization: Department of Medical Biotechnology and Laboratory Science, Center for Molecular and Clinical Immunology, College of Medicine, Chang Gung University, Taoyuan, Taiwan – sequence: 3 givenname: Sheng-Hui surname: Tsai fullname: Tsai, Sheng-Hui organization: Department of Medical Biotechnology and Laboratory Science, Center for Molecular and Clinical Immunology, College of Medicine, Chang Gung University, Taoyuan, Taiwan – sequence: 4 givenname: Chuan-Sheng surname: Lin fullname: Lin, Chuan-Sheng organization: Department of Medical Biotechnology and Laboratory Science, Center for Molecular and Clinical Immunology, College of Medicine, Chang Gung University, Taoyuan, Taiwan – sequence: 5 givenname: Chih-Jung surname: Chang fullname: Chang, Chih-Jung organization: Department of Medical Biotechnology and Laboratory Science, Center for Molecular and Clinical Immunology, College of Medicine, Chang Gung University, Taoyuan, Taiwan – sequence: 6 givenname: Chia-Chen surname: Lu fullname: Lu, Chia-Chen organization: Department of Respiratory Therapy, Fu Jen University, New Taipei City, Taiwan – sequence: 7 givenname: Hsiou-Chen surname: Huang fullname: Huang, Hsiou-Chen organization: Graduate Institute of Biotechnology, National Chung Hsing University, Taichung, Taiwan – sequence: 8 givenname: Hsin-Chih surname: Lai fullname: Lai, Hsin-Chih email: hclai@mail.cgu.edu.tw organization: Department of Medical Biotechnology and Laboratory Science, Center for Molecular and Clinical Immunology, College of Medicine, Chang Gung University, Taoyuan, Taiwan |
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Snippet | Swarming motility is a mode of bacterial movement over a solid surface driven by rotating flagella in a coordinated manner. Bacteria can use two-component... |
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SubjectTerms | animal pathogens bacteria bacterial motility Bacterial Proteins - genetics Bacterial Proteins - metabolism biosynthesis Escherichia coli - metabolism Flagella - metabolism flagellum QseBC RssAB Serratia marcescens Serratia marcescens - metabolism Swarming Two-component system virulence |
Title | Cross-talk between bacterial two-component systems drives stepwise regulation of flagellar biosynthesis in swarming development |
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