PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake
ABSTRACTBacteria absorb different forms of iron through various channels to meet their needs. Our previous studies have shown that TseF, a type VI secretion system effector for Fe uptake, facilitates the delivery of outer membrane vesicle-associated Pseudomonas quinolone signal (PQS)-Fe3+ to bacteri...
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American Society for Microbiology
2024-02-01
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| Series: | Microbiology Spectrum |
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| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.03256-23 |
| _version_ | 1797322802001346560 |
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| author | Heng Zhang Jianshe Yang Juanli Cheng Jing Zeng Xin Ma Jinshui Lin |
| author_facet | Heng Zhang Jianshe Yang Juanli Cheng Jing Zeng Xin Ma Jinshui Lin |
| author_sort | Heng Zhang |
| collection | DOAJ |
| description | ABSTRACTBacteria absorb different forms of iron through various channels to meet their needs. Our previous studies have shown that TseF, a type VI secretion system effector for Fe uptake, facilitates the delivery of outer membrane vesicle-associated Pseudomonas quinolone signal (PQS)-Fe3+ to bacterial cells by a process involving the Fe(III) pyochelin receptor FptA and the porin OprF. However, the form in which the PQS-Fe3+ complex enters the periplasm and how it is moved into the cytoplasm remain unclear. Here, we first demonstrate that the PQS-Fe3+ complex enters the cell directly through FptA or OprF. Next, we show that inner membrane transporters such as FptX, PchHI, and FepBCDG are not only necessary for Pseudomonas aeruginosa to absorb PQS-Fe3+ and pyochelin (PCH)-Fe3+ but are also necessary for the virulence of P. aeruginosa toward Galleria mellonella larvae. Furthermore, we suggest that the function of PQS-Fe3+ (but not PQS)-mediated quorum-sensing regulation is dependent on FptX, PchHI, and FepBCDG. Additionally, the findings indicate that unlike FptX, neither FepBCDG nor PchHI play roles in the autoregulatory loop involving PchR, but further deletion of fepBCDG and pchHI can reverse the inactive PchR phenotype caused by fptX deletion and reactivate the expression of the PCH pathway genes under iron-limited conditions. Finally, this work identifies the interaction between FptX, PchHI, and FepBCDG, indicating that a larger complex could be formed to mediate the uptake of PQS-Fe3+ and PCH-Fe3+. These results pave the way for a better understanding of the PQS and PCH iron absorption pathways and provide future directions for research on tackling P. aeruginosa infections.IMPORTANCEPseudomonas aeruginosa has evolved a number of strategies to acquire the iron it needs from its host, with the most common being the synthesis, secretion, and uptake of siderophores such as pyoverdine, pyochelin, and the quorum-sensing signaling molecule Pseudomonas quinolone signal (PQS). However, despite intensive studies of the siderophore uptake pathways of P. aeruginosa, our understanding of how siderophores transport iron across the inner membrane into the cytoplasm is still incomplete. Herein, we reveal that PQS and pyochelin in P. aeruginosa share inner membrane transporters such as FptX, PchHI, and FepBCDG to mediate iron uptake. Meanwhile, PQS and pyochelin-mediated signaling operate to a large extent via these inner membrane transporters. Our study revealed the existence of shared uptake pathways between PQS and pyochelin, which could lead us to reexamine the role of these two molecules in the iron uptake and virulence of P. aeruginosa. |
| first_indexed | 2024-03-08T05:19:29Z |
| format | Article |
| id | doaj.art-f02e5494e38c465a888fa307c527195c |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-08T05:19:29Z |
| publishDate | 2024-02-01 |
| publisher | American Society for Microbiology |
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| series | Microbiology Spectrum |
| spelling | doaj.art-f02e5494e38c465a888fa307c527195c2024-02-06T14:04:55ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-02-0112210.1128/spectrum.03256-23PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptakeHeng Zhang0Jianshe Yang1Juanli Cheng2Jing Zeng3Xin Ma4Jinshui Lin5Shaanxi Key Laboratory of Chinese Jujube, College of Life Sciences, Yan’an University, Yan’an, ChinaShaanxi Key Laboratory of Chinese Jujube, College of Life Sciences, Yan’an University, Yan’an, ChinaShaanxi Key Laboratory of Chinese Jujube, College of Life Sciences, Yan’an University, Yan’an, ChinaShaanxi Key Laboratory of Chinese Jujube, College of Life Sciences, Yan’an University, Yan’an, ChinaShaanxi Key Laboratory of Chinese Jujube, College of Life Sciences, Yan’an University, Yan’an, ChinaShaanxi Key Laboratory of Chinese Jujube, College of Life Sciences, Yan’an University, Yan’an, ChinaABSTRACTBacteria absorb different forms of iron through various channels to meet their needs. Our previous studies have shown that TseF, a type VI secretion system effector for Fe uptake, facilitates the delivery of outer membrane vesicle-associated Pseudomonas quinolone signal (PQS)-Fe3+ to bacterial cells by a process involving the Fe(III) pyochelin receptor FptA and the porin OprF. However, the form in which the PQS-Fe3+ complex enters the periplasm and how it is moved into the cytoplasm remain unclear. Here, we first demonstrate that the PQS-Fe3+ complex enters the cell directly through FptA or OprF. Next, we show that inner membrane transporters such as FptX, PchHI, and FepBCDG are not only necessary for Pseudomonas aeruginosa to absorb PQS-Fe3+ and pyochelin (PCH)-Fe3+ but are also necessary for the virulence of P. aeruginosa toward Galleria mellonella larvae. Furthermore, we suggest that the function of PQS-Fe3+ (but not PQS)-mediated quorum-sensing regulation is dependent on FptX, PchHI, and FepBCDG. Additionally, the findings indicate that unlike FptX, neither FepBCDG nor PchHI play roles in the autoregulatory loop involving PchR, but further deletion of fepBCDG and pchHI can reverse the inactive PchR phenotype caused by fptX deletion and reactivate the expression of the PCH pathway genes under iron-limited conditions. Finally, this work identifies the interaction between FptX, PchHI, and FepBCDG, indicating that a larger complex could be formed to mediate the uptake of PQS-Fe3+ and PCH-Fe3+. These results pave the way for a better understanding of the PQS and PCH iron absorption pathways and provide future directions for research on tackling P. aeruginosa infections.IMPORTANCEPseudomonas aeruginosa has evolved a number of strategies to acquire the iron it needs from its host, with the most common being the synthesis, secretion, and uptake of siderophores such as pyoverdine, pyochelin, and the quorum-sensing signaling molecule Pseudomonas quinolone signal (PQS). However, despite intensive studies of the siderophore uptake pathways of P. aeruginosa, our understanding of how siderophores transport iron across the inner membrane into the cytoplasm is still incomplete. Herein, we reveal that PQS and pyochelin in P. aeruginosa share inner membrane transporters such as FptX, PchHI, and FepBCDG to mediate iron uptake. Meanwhile, PQS and pyochelin-mediated signaling operate to a large extent via these inner membrane transporters. Our study revealed the existence of shared uptake pathways between PQS and pyochelin, which could lead us to reexamine the role of these two molecules in the iron uptake and virulence of P. aeruginosa.https://journals.asm.org/doi/10.1128/spectrum.03256-23Pseudomonas aeruginosaPQSpyochelininner membrane transporteriron uptake |
| spellingShingle | Heng Zhang Jianshe Yang Juanli Cheng Jing Zeng Xin Ma Jinshui Lin PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake Microbiology Spectrum Pseudomonas aeruginosa PQS pyochelin inner membrane transporter iron uptake |
| title | PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake |
| title_full | PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake |
| title_fullStr | PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake |
| title_full_unstemmed | PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake |
| title_short | PQS and pyochelin in Pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake |
| title_sort | pqs and pyochelin in pseudomonas aeruginosa share inner membrane transporters to mediate iron uptake |
| topic | Pseudomonas aeruginosa PQS pyochelin inner membrane transporter iron uptake |
| url | https://journals.asm.org/doi/10.1128/spectrum.03256-23 |
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