Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24
ABSTRACT Signaling between rhizosphere microorganisms is crucial in bacteria interaction and communication, shaping the rhizomicrobiome. Plant growth-promoting bacterium Pseudomonas produces a spectrum of important antibiotics to inhibit plant pathogens, albeit with an associated metabolic burden. A...
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American Society for Microbiology
2025-03-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01886-24 |
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| author | Nannan Zhang Xianfeng Zhu Xuanying Tao Jie Li Qi Tang Xiaochun Liu Li-Ming Luo Pingping Zhang Li-Qun Zhang Yong-Xing He Honghua Ge |
| author_facet | Nannan Zhang Xianfeng Zhu Xuanying Tao Jie Li Qi Tang Xiaochun Liu Li-Ming Luo Pingping Zhang Li-Qun Zhang Yong-Xing He Honghua Ge |
| author_sort | Nannan Zhang |
| collection | DOAJ |
| description | ABSTRACT Signaling between rhizosphere microorganisms is crucial in bacteria interaction and communication, shaping the rhizomicrobiome. Plant growth-promoting bacterium Pseudomonas produces a spectrum of important antibiotics to inhibit plant pathogens, albeit with an associated metabolic burden. Antibiotics could function as intra- and interspecies signals at subinhibitory concentrations to coordinate gene expression and microbial behaviors. In this work, we characterized pyoluteorin as an interspecies signal that modulates the biosynthesis of 2,4-diacetylphloroglucinol (2,4-DAPG), a broad-spectrum biocontrol agent, in non-pyoluteorin-producing Pseudomonas fluorescens 2P24. We demonstrated that the key transcriptional repressor PhlF from the 2,4-DAPG biosynthetic gene cluster spontaneously senses pyoluteorin, enhancing repression of the phlA promoter activity and inhibiting 2,4-DAPG synthesis in P. fluorescens 2P24. Pyoluteorin also binds to another transcriptional repressor, PhlH, from the 2,4-DAPG biosynthetic gene cluster, subsequently releasing the transcription of phlG, which facilitates the hydrolysis of 2,4-DAPG. Both PhlF and PhlH are simultaneously involved in sensing exogenous pyoluteorin to regulate the 2,4-DAPG biosynthetic operon, playing a crucial role in controlling antibiotic metabolites in response to environmental changes. Further phylogenetic and structural analyses demonstrated that PhlH and PhlF are widely distributed across Pseudomonas spp. with conserved ligand-binding domains. The findings shed new light on the regulatory mechanism of 2,4-DAPG biosynthesis underlying interspecies signaling by pyoluteorin and provide invaluable clues for the rational design of co-inhabiting Pseudomonas spp. as biocontrol agents.IMPORTANCERhizosphere microorganisms release vital signals that shape microbial communities, with antibiotics at low concentrations acting as intra- and interspecies signals. However, the mechanisms of these signals in coordinating gene expression are unclear. In non-pyoluteorin-producing Pseudomonas fluorescens 2P24, pyoluteorin was identified as an interspecies signal that regulates the phl biosynthesis gene cluster for 2,4-DAPG production. TetR family repressors PhlH and PhlF were found to positively regulate 2,4-DAPG hydrolysis and negatively regulate its synthesis in response to pyoluteorin. Structural modeling and docking analyses revealed the interactions between pyoluteorin and both PhlH and PhlF, modulating gene expression. Phylogenetic analyses showed a wide distribution of PhlH and PhlF across Pseudomonas spp. with conserved ligand-binding domains. These findings deepen our understanding of interspecies signaling mechanisms and highlight the potential for designing co-inhabiting Pseudomonas spp. as effective biocontrol agents. |
| format | Article |
| id | doaj-art-1909162c6d5f4378b0e2ce032a5e3280 |
| institution | OA Journals |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | American Society for Microbiology |
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| series | Microbiology Spectrum |
| spelling | doaj-art-1909162c6d5f4378b0e2ce032a5e32802025-08-20T02:02:09ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-03-0113310.1128/spectrum.01886-24Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24Nannan Zhang0Xianfeng Zhu1Xuanying Tao2Jie Li3Qi Tang4Xiaochun Liu5Li-Ming Luo6Pingping Zhang7Li-Qun Zhang8Yong-Xing He9Honghua Ge10School of Life Sciences, Anhui University, Hefei, ChinaInstitute of Health Sciences and Technology, Anhui University, Hefei, ChinaSchool of Life Sciences, Anhui University, Hefei, ChinaInstitute of Health Sciences and Technology, Anhui University, Hefei, ChinaInstitute of Health Sciences and Technology, Anhui University, Hefei, ChinaInstitute of Health Sciences and Technology, Anhui University, Hefei, ChinaMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou, ChinaSchool of Life Sciences, Anhui University, Hefei, ChinaCollege of Plant Protection, China Agricultural University, Beijing, ChinaMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou, ChinaSchool of Life Sciences, Anhui University, Hefei, ChinaABSTRACT Signaling between rhizosphere microorganisms is crucial in bacteria interaction and communication, shaping the rhizomicrobiome. Plant growth-promoting bacterium Pseudomonas produces a spectrum of important antibiotics to inhibit plant pathogens, albeit with an associated metabolic burden. Antibiotics could function as intra- and interspecies signals at subinhibitory concentrations to coordinate gene expression and microbial behaviors. In this work, we characterized pyoluteorin as an interspecies signal that modulates the biosynthesis of 2,4-diacetylphloroglucinol (2,4-DAPG), a broad-spectrum biocontrol agent, in non-pyoluteorin-producing Pseudomonas fluorescens 2P24. We demonstrated that the key transcriptional repressor PhlF from the 2,4-DAPG biosynthetic gene cluster spontaneously senses pyoluteorin, enhancing repression of the phlA promoter activity and inhibiting 2,4-DAPG synthesis in P. fluorescens 2P24. Pyoluteorin also binds to another transcriptional repressor, PhlH, from the 2,4-DAPG biosynthetic gene cluster, subsequently releasing the transcription of phlG, which facilitates the hydrolysis of 2,4-DAPG. Both PhlF and PhlH are simultaneously involved in sensing exogenous pyoluteorin to regulate the 2,4-DAPG biosynthetic operon, playing a crucial role in controlling antibiotic metabolites in response to environmental changes. Further phylogenetic and structural analyses demonstrated that PhlH and PhlF are widely distributed across Pseudomonas spp. with conserved ligand-binding domains. The findings shed new light on the regulatory mechanism of 2,4-DAPG biosynthesis underlying interspecies signaling by pyoluteorin and provide invaluable clues for the rational design of co-inhabiting Pseudomonas spp. as biocontrol agents.IMPORTANCERhizosphere microorganisms release vital signals that shape microbial communities, with antibiotics at low concentrations acting as intra- and interspecies signals. However, the mechanisms of these signals in coordinating gene expression are unclear. In non-pyoluteorin-producing Pseudomonas fluorescens 2P24, pyoluteorin was identified as an interspecies signal that regulates the phl biosynthesis gene cluster for 2,4-DAPG production. TetR family repressors PhlH and PhlF were found to positively regulate 2,4-DAPG hydrolysis and negatively regulate its synthesis in response to pyoluteorin. Structural modeling and docking analyses revealed the interactions between pyoluteorin and both PhlH and PhlF, modulating gene expression. Phylogenetic analyses showed a wide distribution of PhlH and PhlF across Pseudomonas spp. with conserved ligand-binding domains. These findings deepen our understanding of interspecies signaling mechanisms and highlight the potential for designing co-inhabiting Pseudomonas spp. as effective biocontrol agents.https://journals.asm.org/doi/10.1128/spectrum.01886-24Pseudomonaspyoluteorininterspecies signalingtranscriptional repressor2,4-diacetylphloroglucinol |
| spellingShingle | Nannan Zhang Xianfeng Zhu Xuanying Tao Jie Li Qi Tang Xiaochun Liu Li-Ming Luo Pingping Zhang Li-Qun Zhang Yong-Xing He Honghua Ge Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24 Microbiology Spectrum Pseudomonas pyoluteorin interspecies signaling transcriptional repressor 2,4-diacetylphloroglucinol |
| title | Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24 |
| title_full | Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24 |
| title_fullStr | Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24 |
| title_full_unstemmed | Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24 |
| title_short | Interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of Pseudomonas fluorescens 2P24 |
| title_sort | interspecies signaling modulates the biosynthesis of antimicrobial secondary metabolites related to biological control activities of pseudomonas fluorescens 2p24 |
| topic | Pseudomonas pyoluteorin interspecies signaling transcriptional repressor 2,4-diacetylphloroglucinol |
| url | https://journals.asm.org/doi/10.1128/spectrum.01886-24 |
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