Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosa
ABSTRACT Pseudomonas aeruginosa is a vital opportunistic human bacterial pathogen that causes acute and chronic infections. In this study, we set to determine whether the endogenous spermidine biosynthesis plays a role in regulation of type III secretion system (T3SS). The results showed that deleti...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00644-22 |
| _version_ | 1811238126657470464 |
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| author | Qiqi Lin Huishan Wang Jiahui Huang Zhiqing Liu Qunyi Chen Guohui Yu Zeling Xu Ping Cheng Zhibin Liang Lian-Hui Zhang |
| author_facet | Qiqi Lin Huishan Wang Jiahui Huang Zhiqing Liu Qunyi Chen Guohui Yu Zeling Xu Ping Cheng Zhibin Liang Lian-Hui Zhang |
| author_sort | Qiqi Lin |
| collection | DOAJ |
| description | ABSTRACT Pseudomonas aeruginosa is a vital opportunistic human bacterial pathogen that causes acute and chronic infections. In this study, we set to determine whether the endogenous spermidine biosynthesis plays a role in regulation of type III secretion system (T3SS). The results showed that deletion of speA and speC, which encode putrescine biosynthesis, did not seem to affect cellular spermidine level and the T3SS gene expression. In contrast, mutation of speD and speE encoding spermidine biosynthesis led to significantly decreased spermidine production and expression of T3SS genes. We also showed that endogenous spermidine could auto-induce the transcriptional expression of speE and its full functionality required the transporter SpuDEFGH. Cytotoxicity analysis showed that mutants ΔspeE and ΔspuE were substantially attenuated in virulence compared with their wild-type strain PAO1. Our data imply a possibility that spermidine biosynthesis in P. aeruginosa may not use putrescine as a substrate, and that spermidine signaling pathway may interact with other two T3SS regulatory mechanisms in certain degree, i.e., cAMP-Vfr and GacS/GacA signaling systems. Taken together, these results specify the role of endogenous spermidine in regulation of T3SS in P. aeruginosa and provide useful clues for design and development antimicrobial therapies. IMPORTANCE Type III secretion system (T3SS) is one of the pivotal virulence factors of Pseudomonas aeruginosa responsible for evading phagocytosis, and secreting and translocating effectors into host cells. Previous studies underline the complicated and elaborate regulatory mechanisms of T3SS for the accurate, fast, and malicious pathogenicity of P. aeruginosa. Among these regulatory mechanisms, our previous study indicated that the spermidine from the host was vital to the host-pathogen interaction. However, the role of endogenous spermidine synthesized by P. aeruginosa on the regulation of T3SS expression is largely unknown. Here we reveal the role and regulatory network of endogenous spermidine synthesis in regulation of T3SS and bacterial virulence, showing that the spermidine is an important interspecies signal for modulating the virulence of P. aeruginosa through regulating T3SS expression. |
| first_indexed | 2024-04-12T12:36:21Z |
| format | Article |
| id | doaj.art-700c048102ae43c686644201b25e47e0 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-12T12:36:21Z |
| publishDate | 2022-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-700c048102ae43c686644201b25e47e02022-12-22T03:32:54ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-06-0110310.1128/spectrum.00644-22Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosaQiqi Lin0Huishan Wang1Jiahui Huang2Zhiqing Liu3Qunyi Chen4Guohui Yu5Zeling Xu6Ping Cheng7Zhibin Liang8Lian-Hui Zhang9Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaInstitute of Plant Health, Zhongkai University of Agriculture and Engineering, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaInstitute of Plant Health, Zhongkai University of Agriculture and Engineering, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University, Guangzhou, ChinaABSTRACT Pseudomonas aeruginosa is a vital opportunistic human bacterial pathogen that causes acute and chronic infections. In this study, we set to determine whether the endogenous spermidine biosynthesis plays a role in regulation of type III secretion system (T3SS). The results showed that deletion of speA and speC, which encode putrescine biosynthesis, did not seem to affect cellular spermidine level and the T3SS gene expression. In contrast, mutation of speD and speE encoding spermidine biosynthesis led to significantly decreased spermidine production and expression of T3SS genes. We also showed that endogenous spermidine could auto-induce the transcriptional expression of speE and its full functionality required the transporter SpuDEFGH. Cytotoxicity analysis showed that mutants ΔspeE and ΔspuE were substantially attenuated in virulence compared with their wild-type strain PAO1. Our data imply a possibility that spermidine biosynthesis in P. aeruginosa may not use putrescine as a substrate, and that spermidine signaling pathway may interact with other two T3SS regulatory mechanisms in certain degree, i.e., cAMP-Vfr and GacS/GacA signaling systems. Taken together, these results specify the role of endogenous spermidine in regulation of T3SS in P. aeruginosa and provide useful clues for design and development antimicrobial therapies. IMPORTANCE Type III secretion system (T3SS) is one of the pivotal virulence factors of Pseudomonas aeruginosa responsible for evading phagocytosis, and secreting and translocating effectors into host cells. Previous studies underline the complicated and elaborate regulatory mechanisms of T3SS for the accurate, fast, and malicious pathogenicity of P. aeruginosa. Among these regulatory mechanisms, our previous study indicated that the spermidine from the host was vital to the host-pathogen interaction. However, the role of endogenous spermidine synthesized by P. aeruginosa on the regulation of T3SS expression is largely unknown. Here we reveal the role and regulatory network of endogenous spermidine synthesis in regulation of T3SS and bacterial virulence, showing that the spermidine is an important interspecies signal for modulating the virulence of P. aeruginosa through regulating T3SS expression.https://journals.asm.org/doi/10.1128/spectrum.00644-22spermidineexsCEBAT3SSregulationquorum sensingspermidine |
| spellingShingle | Qiqi Lin Huishan Wang Jiahui Huang Zhiqing Liu Qunyi Chen Guohui Yu Zeling Xu Ping Cheng Zhibin Liang Lian-Hui Zhang Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosa Microbiology Spectrum spermidine exsCEBA T3SS regulation quorum sensing spermidine |
| title | Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosa |
| title_full | Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosa |
| title_fullStr | Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosa |
| title_full_unstemmed | Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosa |
| title_short | Spermidine Is an Intercellular Signal Modulating T3SS Expression in Pseudomonas aeruginosa |
| title_sort | spermidine is an intercellular signal modulating t3ss expression in pseudomonas aeruginosa |
| topic | spermidine exsCEBA T3SS regulation quorum sensing spermidine |
| url | https://journals.asm.org/doi/10.1128/spectrum.00644-22 |
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