Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent Growth
In Escherichia coli, repression of phosphatidylglycerol synthase A gene (pgsA) lowers the levels of membrane acidic phospholipids, particularly phosphatidylglycerol (PG), causing growth-arrested phenotype. The interrupted synthesis of PG is known to be associated with concomitant reduction of chromo...
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Frontiers Media S.A.
2021-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.677812/full |
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| author | Digvijay Patil Dan Xun Markus Schueritz Shivani Bansal Amrita Cheema Elliott Crooke Elliott Crooke Rahul Saxena |
| author_facet | Digvijay Patil Dan Xun Markus Schueritz Shivani Bansal Amrita Cheema Elliott Crooke Elliott Crooke Rahul Saxena |
| author_sort | Digvijay Patil |
| collection | DOAJ |
| description | In Escherichia coli, repression of phosphatidylglycerol synthase A gene (pgsA) lowers the levels of membrane acidic phospholipids, particularly phosphatidylglycerol (PG), causing growth-arrested phenotype. The interrupted synthesis of PG is known to be associated with concomitant reduction of chromosomal content and cell mass, in addition to accumulation of unprocessed outer membrane lipoprotein intermediate, pro-Lpp, at the inner membrane. However, whether a linkage exists between the two altered-membrane outcomes remains unknown. Previously, it has been shown that pgsA+ cells overexpressing mutant Lpp(C21G) protein have growth defects similar to those caused by the unprocessed pro-Lpp intermediate in cells lacking PG. Here, we found that the ectopic expression of DnaA(L366K) or deletion of fis (encoding Factor for Inversion Stimulation) permits growth of cells that otherwise would be arrested for growth due to accumulated Lpp(C21G). The DnaA(L366K)-mediated restoration of growth occurs by reduced expression of Lpp(C21G) via a σE-dependent small-regulatory RNA (sRNA), MicL-S. In contrast, restoration of growth via fis deletion is only partially dependent on the MicL-S pathway; deletion of fis also rescues Lpp(C21G) growth arrest in cells lacking physiological levels of PG and cardiolipin (CL), independently of MicL-S. Our results suggest a close link between the physiological state of the bacterial cell membrane and DnaA- and Fis-dependent growth. |
| first_indexed | 2024-12-19T03:47:53Z |
| format | Article |
| id | doaj.art-fb831c894c8747ad980fb68f79363042 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-19T03:47:53Z |
| publishDate | 2021-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-fb831c894c8747ad980fb68f793630422022-12-21T20:37:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-06-011210.3389/fmicb.2021.677812677812Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent GrowthDigvijay Patil0Dan Xun1Markus Schueritz2Shivani Bansal3Amrita Cheema4Elliott Crooke5Elliott Crooke6Rahul Saxena7Department of Biochemistry and Molecular and Cellular Biology, Georgetown University Medical Center, Washington, DC, United StatesDepartment of Biochemistry and Molecular and Cellular Biology, Georgetown University Medical Center, Washington, DC, United StatesDepartment of Biochemistry and Molecular and Cellular Biology, Georgetown University Medical Center, Washington, DC, United StatesLombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington DC, United StatesLombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington DC, United StatesDepartment of Biochemistry and Molecular and Cellular Biology, Georgetown University Medical Center, Washington, DC, United StatesLombardi Comprehensive Cancer Center, Georgetown University Medical Center, Washington DC, United StatesDepartment of Biochemistry and Molecular and Cellular Biology, Georgetown University Medical Center, Washington, DC, United StatesIn Escherichia coli, repression of phosphatidylglycerol synthase A gene (pgsA) lowers the levels of membrane acidic phospholipids, particularly phosphatidylglycerol (PG), causing growth-arrested phenotype. The interrupted synthesis of PG is known to be associated with concomitant reduction of chromosomal content and cell mass, in addition to accumulation of unprocessed outer membrane lipoprotein intermediate, pro-Lpp, at the inner membrane. However, whether a linkage exists between the two altered-membrane outcomes remains unknown. Previously, it has been shown that pgsA+ cells overexpressing mutant Lpp(C21G) protein have growth defects similar to those caused by the unprocessed pro-Lpp intermediate in cells lacking PG. Here, we found that the ectopic expression of DnaA(L366K) or deletion of fis (encoding Factor for Inversion Stimulation) permits growth of cells that otherwise would be arrested for growth due to accumulated Lpp(C21G). The DnaA(L366K)-mediated restoration of growth occurs by reduced expression of Lpp(C21G) via a σE-dependent small-regulatory RNA (sRNA), MicL-S. In contrast, restoration of growth via fis deletion is only partially dependent on the MicL-S pathway; deletion of fis also rescues Lpp(C21G) growth arrest in cells lacking physiological levels of PG and cardiolipin (CL), independently of MicL-S. Our results suggest a close link between the physiological state of the bacterial cell membrane and DnaA- and Fis-dependent growth.https://www.frontiersin.org/articles/10.3389/fmicb.2021.677812/fullEscherichia coliDNA replicationacidic phospholipidslipoprotein biogenesisDnaAFis |
| spellingShingle | Digvijay Patil Dan Xun Markus Schueritz Shivani Bansal Amrita Cheema Elliott Crooke Elliott Crooke Rahul Saxena Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent Growth Frontiers in Microbiology Escherichia coli DNA replication acidic phospholipids lipoprotein biogenesis DnaA Fis |
| title | Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent Growth |
| title_full | Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent Growth |
| title_fullStr | Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent Growth |
| title_full_unstemmed | Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent Growth |
| title_short | Membrane Stress Caused by Unprocessed Outer Membrane Lipoprotein Intermediate Pro-Lpp Affects DnaA and Fis-Dependent Growth |
| title_sort | membrane stress caused by unprocessed outer membrane lipoprotein intermediate pro lpp affects dnaa and fis dependent growth |
| topic | Escherichia coli DNA replication acidic phospholipids lipoprotein biogenesis DnaA Fis |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.677812/full |
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