A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veronii
IntroductionResponse regulators from diverse two-component systems often function as diguanylate cyclases or phosphodiesterases, thereby enabling precise regulation of intracellular c-di-GMP levels to control bacterial virulence and motility. However, the regulatory mechanisms of c-di-GMP require fu...
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Frontiers Media S.A.
2025-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1527317/full |
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| author | Chaolun Liu Jia Shao Xiang Ma Yanqiong Tang Juanjuan Li Hong Li Xue Chi Zhu Liu |
| author_facet | Chaolun Liu Jia Shao Xiang Ma Yanqiong Tang Juanjuan Li Hong Li Xue Chi Zhu Liu |
| author_sort | Chaolun Liu |
| collection | DOAJ |
| description | IntroductionResponse regulators from diverse two-component systems often function as diguanylate cyclases or phosphodiesterases, thereby enabling precise regulation of intracellular c-di-GMP levels to control bacterial virulence and motility. However, the regulatory mechanisms of c-di-GMP require further elucidation.MethodsThis study confirmed that ArrS and ArrR form a two-component system via structural analysis, two-hybrid, and phosphodiesterase activity detection. To evaluate the impact of ArrS/ArrR on intracellular c-di-GMP levels, biofilm detection, motility detection, fluorescence reporter plasmids, and LC-MS/MS analysis were employed. One-hybrid, EMSA, and RT-qPCR were used to demonstrate the function of ArgR on arrSR promoter. The roles of ArrS/ArrR in Aeromonas veronii were investigated using RT-qPCR, murine model, and proteomics.ResultsArrS and ArrR constituted a two-component system in Aeromonas veronii and were transcriptionally repressed by ArgR. ArrR exhibited phosphodiesterase activity, which is inhibited through phosphorylation mediated by ArrS. In Aeromonas veronii, ArrS/ArrR significantly altered the intracellular c-di-GMP levels. In a murine model, ΔarrS exhibited increased pathogenicity, leading to elevated TNF-α and IFN-γ levels in serum, and severer toxicity to spleen and kidney. These effects might be elucidated by the upregulated inflammation-associated proteins in ΔarrS. Moreover, the exonuclease RecB was also up-regulated in ΔarrS.DiscussionWe elucidated the regulatory mechanism of ArrS/ArrR on intracellular c-di-GMP levels and its impact on the virulence in Aeromonas veronii, and discussed the intricate relationship between c-di-GMP metabolism and arginine metabolism. |
| format | Article |
| id | doaj-art-3c2be98dcef847499f119aef5fc30fd2 |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj-art-3c2be98dcef847499f119aef5fc30fd22025-01-30T16:01:29ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011610.3389/fmicb.2025.15273171527317A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veroniiChaolun LiuJia ShaoXiang MaYanqiong TangJuanjuan LiHong LiXue ChiZhu LiuIntroductionResponse regulators from diverse two-component systems often function as diguanylate cyclases or phosphodiesterases, thereby enabling precise regulation of intracellular c-di-GMP levels to control bacterial virulence and motility. However, the regulatory mechanisms of c-di-GMP require further elucidation.MethodsThis study confirmed that ArrS and ArrR form a two-component system via structural analysis, two-hybrid, and phosphodiesterase activity detection. To evaluate the impact of ArrS/ArrR on intracellular c-di-GMP levels, biofilm detection, motility detection, fluorescence reporter plasmids, and LC-MS/MS analysis were employed. One-hybrid, EMSA, and RT-qPCR were used to demonstrate the function of ArgR on arrSR promoter. The roles of ArrS/ArrR in Aeromonas veronii were investigated using RT-qPCR, murine model, and proteomics.ResultsArrS and ArrR constituted a two-component system in Aeromonas veronii and were transcriptionally repressed by ArgR. ArrR exhibited phosphodiesterase activity, which is inhibited through phosphorylation mediated by ArrS. In Aeromonas veronii, ArrS/ArrR significantly altered the intracellular c-di-GMP levels. In a murine model, ΔarrS exhibited increased pathogenicity, leading to elevated TNF-α and IFN-γ levels in serum, and severer toxicity to spleen and kidney. These effects might be elucidated by the upregulated inflammation-associated proteins in ΔarrS. Moreover, the exonuclease RecB was also up-regulated in ΔarrS.DiscussionWe elucidated the regulatory mechanism of ArrS/ArrR on intracellular c-di-GMP levels and its impact on the virulence in Aeromonas veronii, and discussed the intricate relationship between c-di-GMP metabolism and arginine metabolism.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1527317/fullAeromonas veroniitwo-component systemc-di-GMPphosphodiesterasemotilityArgR |
| spellingShingle | Chaolun Liu Jia Shao Xiang Ma Yanqiong Tang Juanjuan Li Hong Li Xue Chi Zhu Liu A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veronii Frontiers in Microbiology Aeromonas veronii two-component system c-di-GMP phosphodiesterase motility ArgR |
| title | A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veronii |
| title_full | A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veronii |
| title_fullStr | A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veronii |
| title_full_unstemmed | A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veronii |
| title_short | A novel two-component system contributing the catabolism of c-di-GMP influences virulence in Aeromonas veronii |
| title_sort | novel two component system contributing the catabolism of c di gmp influences virulence in aeromonas veronii |
| topic | Aeromonas veronii two-component system c-di-GMP phosphodiesterase motility ArgR |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2025.1527317/full |
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