Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24
Abstract The coordination of public and private goods production is essential for bacterial adaptation to environmental changes. Quorum sensing (QS) regulates this balance by mediating the trade‐off between the communal benefits of “public goods,” such as siderophores and antibiotics, and the indivi...
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Wiley
2025-03-01
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| Series: | Advanced Science |
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| Online Access: | https://doi.org/10.1002/advs.202412224 |
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| author | Jie Li Mengxue Nie Hongguang Ma Xuanying Tao Yanxia Sun Xinyue Tu Pingping Zhang Li‐Qun Zhang Rong Jia Yong‐Xing He Nannan Zhang Honghua Ge |
| author_facet | Jie Li Mengxue Nie Hongguang Ma Xuanying Tao Yanxia Sun Xinyue Tu Pingping Zhang Li‐Qun Zhang Rong Jia Yong‐Xing He Nannan Zhang Honghua Ge |
| author_sort | Jie Li |
| collection | DOAJ |
| description | Abstract The coordination of public and private goods production is essential for bacterial adaptation to environmental changes. Quorum sensing (QS) regulates this balance by mediating the trade‐off between the communal benefits of “public goods,” such as siderophores and antibiotics, and the individual metabolic needs fulfilled by “private goods,” such as intracellular metabolites utilized for growth and survival. Pseudomonas fluorescens 2P24 harbors a LasI/LasR‐type QS system, MupI/MupR, which regulates mupirocin production through signaling molecules. This study explores how QS coordinates carbon and nitrogen metabolism to optimize the production of key secondary metabolites, including 2,4‐diacetylphloroglucinol (2,4‐DAPG), mupirocin, and siderophores, which serve as public goods. Loss of QS disrupts this balance by enhancing the Krebs cycle, denitrification, pyruvate anaplerosis, and ammonium assimilation, lead to halted 2,4‐DAPG and mupirocin synthesis and increased siderophore production. In the absence of QS, elevated siderophore production compensates for iron acquisition, ensuring rapid cellular growth. Under nutrient‐limited or high cell density conditions, MupR regulates carbon and nitrogen fluxes to sustain public goods production. These findings highlight QS as a key environmental sensor that fine‐tunes resource allocation, bacterial fitness, and adaptation to ecological and nutritional conditions, suggesting the potential for QS‐targeted approaches to enhance antibiotic production and agricultural sustainability. |
| format | Article |
| id | doaj-art-25f340fdf8684c47987c97e9b75c0cdf |
| institution | OA Journals |
| issn | 2198-3844 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | Wiley |
| record_format | Article |
| series | Advanced Science |
| spelling | doaj-art-25f340fdf8684c47987c97e9b75c0cdf2025-08-20T02:10:46ZengWileyAdvanced Science2198-38442025-03-011212n/an/a10.1002/advs.202412224Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24Jie Li0Mengxue Nie1Hongguang Ma2Xuanying Tao3Yanxia Sun4Xinyue Tu5Pingping Zhang6Li‐Qun Zhang7Rong Jia8Yong‐Xing He9Nannan Zhang10Honghua Ge11School of Life Sciences Anhui University Hefei 230601 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaCollege of Plant Protection China Agricultural University Beijing 100083 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaMinistry of Education Key Laboratory of Cell Activities and Stress Adaptations School of Life Sciences Lanzhou University Lanzhou 730000 ChinaSchool of Life Sciences Anhui University Hefei 230601 ChinaInstitute of Health Sciences and Technology Institutes of Physical Science and Information Technology Anhui University Hefei 230601 ChinaAbstract The coordination of public and private goods production is essential for bacterial adaptation to environmental changes. Quorum sensing (QS) regulates this balance by mediating the trade‐off between the communal benefits of “public goods,” such as siderophores and antibiotics, and the individual metabolic needs fulfilled by “private goods,” such as intracellular metabolites utilized for growth and survival. Pseudomonas fluorescens 2P24 harbors a LasI/LasR‐type QS system, MupI/MupR, which regulates mupirocin production through signaling molecules. This study explores how QS coordinates carbon and nitrogen metabolism to optimize the production of key secondary metabolites, including 2,4‐diacetylphloroglucinol (2,4‐DAPG), mupirocin, and siderophores, which serve as public goods. Loss of QS disrupts this balance by enhancing the Krebs cycle, denitrification, pyruvate anaplerosis, and ammonium assimilation, lead to halted 2,4‐DAPG and mupirocin synthesis and increased siderophore production. In the absence of QS, elevated siderophore production compensates for iron acquisition, ensuring rapid cellular growth. Under nutrient‐limited or high cell density conditions, MupR regulates carbon and nitrogen fluxes to sustain public goods production. These findings highlight QS as a key environmental sensor that fine‐tunes resource allocation, bacterial fitness, and adaptation to ecological and nutritional conditions, suggesting the potential for QS‐targeted approaches to enhance antibiotic production and agricultural sustainability.https://doi.org/10.1002/advs.202412224carbon and nitrogen metabolismgene transcriptionpublic goodsquorum sensingtranscription factor |
| spellingShingle | Jie Li Mengxue Nie Hongguang Ma Xuanying Tao Yanxia Sun Xinyue Tu Pingping Zhang Li‐Qun Zhang Rong Jia Yong‐Xing He Nannan Zhang Honghua Ge Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24 Advanced Science carbon and nitrogen metabolism gene transcription public goods quorum sensing transcription factor |
| title | Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24 |
| title_full | Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24 |
| title_fullStr | Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24 |
| title_full_unstemmed | Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24 |
| title_short | Quorum Sensing Coordinates Carbon and Nitrogen Metabolism to Optimize Public Goods Production in Pseudomonas fluorescens 2P24 |
| title_sort | quorum sensing coordinates carbon and nitrogen metabolism to optimize public goods production in pseudomonas fluorescens 2p24 |
| topic | carbon and nitrogen metabolism gene transcription public goods quorum sensing transcription factor |
| url | https://doi.org/10.1002/advs.202412224 |
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