Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expression
ABSTRACT Glaesserella parasuis, a common inhabitant of the upper respiratory tract of pigs, is the etiological agent of Glässer’s disease, which is characterized by fibrinous polyserositis, polyarthritis, and meningitis. Decreased production of capsular polysaccharide (CPS) promotes bacterial adhesi...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-12-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01508-23 |
| _version_ | 1797393688370872320 |
|---|---|
| author | Ju Sun Siting Wen Zhichao Wang Wei Liu Yan Lin Jiayun Gu Weiting Mao Xiaojuan Xu Qigai He Xuwang Cai |
| author_facet | Ju Sun Siting Wen Zhichao Wang Wei Liu Yan Lin Jiayun Gu Weiting Mao Xiaojuan Xu Qigai He Xuwang Cai |
| author_sort | Ju Sun |
| collection | DOAJ |
| description | ABSTRACT Glaesserella parasuis, a common inhabitant of the upper respiratory tract of pigs, is the etiological agent of Glässer’s disease, which is characterized by fibrinous polyserositis, polyarthritis, and meningitis. Decreased production of capsular polysaccharide (CPS) promotes bacterial adhesion and uptake, whereas maximal expression of CPS is essential to evade the host immune response. For bacterial survival under highly variable host conditions, a coordinated regulation of CPS expression is necessary. In the present study, we investigated how epinephrine (Epi) affects the CPS production, biofilm formation, and adhesion ability of G. parasuis, as well as the specific mechanism of G. parasuis changes in response to Epi. The results demonstrated that Epi stimulation dramatically inhibited CPS expression, and both the action of Epi and the deletion of CPS biosynthesis gene capD had detrimental impacts on biofilm formation, and had the enhanced ability for cell adhesion. QseBC two-component system is a typical adrenaline-sensing system in bacteria. In the present study, by quantitative real-time PCR, Western blot, and electrophoretic mobility shift assay, we discovered that in the presence of Epi, G. parasuis negatively regulated capD expression via the interaction of QseB with the promoter of capD, thereby affecting the synthesis of CPS. In conclusion, we explored the impact of Epi on CPS synthesis and defined its regulatory mechanism in G. parasuis for the first time, which provides an important theoretical basis for understanding the pathogenic mechanism of G. parasuis. IMPORTANCE The key bacterial pathogen Glaesserella parasuis, which can cause Glässer’s disease, has caused significant financial losses to the swine industry worldwide. Capsular polysaccharide (CPS) is an important virulence factor for bacteria, providing the ability to avoid recognition and killing by the host immune system. Exploring the alteration of CPS synthesis in G. parasuis in response to epinephrine stimulation can lay the groundwork for revealing the pathogenic mechanism of G. parasuis as well as providing ideas for Glässer’s disease control. |
| first_indexed | 2024-03-09T00:06:30Z |
| format | Article |
| id | doaj.art-ab49ef0d9d314bb1b5ee0f37dec9613f |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:30Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-ab49ef0d9d314bb1b5ee0f37dec9613f2023-12-12T13:17:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.01508-23Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expressionJu Sun0Siting Wen1Zhichao Wang2Wei Liu3Yan Lin4Jiayun Gu5Weiting Mao6Xiaojuan Xu7Qigai He8Xuwang Cai9National Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University , Wuhan, Hubei, ChinaABSTRACT Glaesserella parasuis, a common inhabitant of the upper respiratory tract of pigs, is the etiological agent of Glässer’s disease, which is characterized by fibrinous polyserositis, polyarthritis, and meningitis. Decreased production of capsular polysaccharide (CPS) promotes bacterial adhesion and uptake, whereas maximal expression of CPS is essential to evade the host immune response. For bacterial survival under highly variable host conditions, a coordinated regulation of CPS expression is necessary. In the present study, we investigated how epinephrine (Epi) affects the CPS production, biofilm formation, and adhesion ability of G. parasuis, as well as the specific mechanism of G. parasuis changes in response to Epi. The results demonstrated that Epi stimulation dramatically inhibited CPS expression, and both the action of Epi and the deletion of CPS biosynthesis gene capD had detrimental impacts on biofilm formation, and had the enhanced ability for cell adhesion. QseBC two-component system is a typical adrenaline-sensing system in bacteria. In the present study, by quantitative real-time PCR, Western blot, and electrophoretic mobility shift assay, we discovered that in the presence of Epi, G. parasuis negatively regulated capD expression via the interaction of QseB with the promoter of capD, thereby affecting the synthesis of CPS. In conclusion, we explored the impact of Epi on CPS synthesis and defined its regulatory mechanism in G. parasuis for the first time, which provides an important theoretical basis for understanding the pathogenic mechanism of G. parasuis. IMPORTANCE The key bacterial pathogen Glaesserella parasuis, which can cause Glässer’s disease, has caused significant financial losses to the swine industry worldwide. Capsular polysaccharide (CPS) is an important virulence factor for bacteria, providing the ability to avoid recognition and killing by the host immune system. Exploring the alteration of CPS synthesis in G. parasuis in response to epinephrine stimulation can lay the groundwork for revealing the pathogenic mechanism of G. parasuis as well as providing ideas for Glässer’s disease control.https://journals.asm.org/doi/10.1128/spectrum.01508-23Glaesserella parasuiscapsular polysaccharideepinephrinetwo-component system |
| spellingShingle | Ju Sun Siting Wen Zhichao Wang Wei Liu Yan Lin Jiayun Gu Weiting Mao Xiaojuan Xu Qigai He Xuwang Cai Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expression Microbiology Spectrum Glaesserella parasuis capsular polysaccharide epinephrine two-component system |
| title | Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expression |
| title_full | Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expression |
| title_fullStr | Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expression |
| title_full_unstemmed | Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expression |
| title_short | Glaesserella parasuis QseBC two-component system senses epinephrine and regulates capD expression |
| title_sort | glaesserella parasuis qsebc two component system senses epinephrine and regulates capd expression |
| topic | Glaesserella parasuis capsular polysaccharide epinephrine two-component system |
| url | https://journals.asm.org/doi/10.1128/spectrum.01508-23 |
| work_keys_str_mv | AT jusun glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT sitingwen glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT zhichaowang glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT weiliu glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT yanlin glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT jiayungu glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT weitingmao glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT xiaojuanxu glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT qigaihe glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression AT xuwangcai glaesserellaparasuisqsebctwocomponentsystemsensesepinephrineandregulatescapdexpression |