A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli
Abstract All free-living microorganisms homeostatically maintain the fluidity of their membranes by adapting lipid composition to environmental temperatures. Here, we quantify enzymes and metabolic intermediates of the Escherichia coli fatty acid and phospholipid synthesis pathways, to describe how...
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Nature Portfolio
2024-10-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-53677-5 |
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| author | Loles Hoogerland Stefan Pieter Hendrik van den Berg Yixing Suo Yuta W. Moriuchi Adja Zoumaro-Djayoon Esther Geurken Flora Yang Frank Bruggeman Michael D. Burkart Gregory Bokinsky |
| author_facet | Loles Hoogerland Stefan Pieter Hendrik van den Berg Yixing Suo Yuta W. Moriuchi Adja Zoumaro-Djayoon Esther Geurken Flora Yang Frank Bruggeman Michael D. Burkart Gregory Bokinsky |
| author_sort | Loles Hoogerland |
| collection | DOAJ |
| description | Abstract All free-living microorganisms homeostatically maintain the fluidity of their membranes by adapting lipid composition to environmental temperatures. Here, we quantify enzymes and metabolic intermediates of the Escherichia coli fatty acid and phospholipid synthesis pathways, to describe how this organism measures temperature and restores optimal membrane fluidity within a single generation after a temperature shock. A first element of this regulatory system is a temperature-sensitive metabolic valve that allocates flux between the saturated and unsaturated fatty acid synthesis pathways via the branchpoint enzymes FabI and FabB. A second element is a transcription-based negative feedback loop that counteracts the temperature-sensitive valve. The combination of these elements accelerates membrane adaptation by causing a transient overshoot in the synthesis of saturated or unsaturated fatty acids following temperature shocks. This strategy is comparable to increasing the temperature of a water bath by adding water that is excessively hot rather than adding water at the desired temperature. These properties are captured in a mathematical model, which we use to show how hard-wired parameters calibrate the system to generate membrane compositions that maintain constant fluidity across temperatures. We hypothesize that core features of the E. coli system will prove to be ubiquitous features of homeoviscous adaptation systems. |
| format | Article |
| id | doaj-art-e815da0745bf4c279554f228a83237fd |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-10-01 |
| publisher | Nature Portfolio |
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| series | Nature Communications |
| spelling | doaj-art-e815da0745bf4c279554f228a83237fd2025-08-20T02:18:35ZengNature PortfolioNature Communications2041-17232024-10-0115111310.1038/s41467-024-53677-5A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coliLoles Hoogerland0Stefan Pieter Hendrik van den Berg1Yixing Suo2Yuta W. Moriuchi3Adja Zoumaro-Djayoon4Esther Geurken5Flora Yang6Frank Bruggeman7Michael D. Burkart8Gregory Bokinsky9Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of TechnologyDepartment of Bionanoscience, Kavli Institute of Nanoscience, Delft University of TechnologyDepartment of Chemistry and Biochemistry, University of CaliforniaDepartment of Chemistry and Biochemistry, University of CaliforniaDepartment of Bionanoscience, Kavli Institute of Nanoscience, Delft University of TechnologyDepartment of Bionanoscience, Kavli Institute of Nanoscience, Delft University of TechnologyDepartment of Bionanoscience, Kavli Institute of Nanoscience, Delft University of TechnologySystems Biology Lab, AIMMS/ALIFE, Vrije Universiteit AmsterdamDepartment of Chemistry and Biochemistry, University of CaliforniaDepartment of Bionanoscience, Kavli Institute of Nanoscience, Delft University of TechnologyAbstract All free-living microorganisms homeostatically maintain the fluidity of their membranes by adapting lipid composition to environmental temperatures. Here, we quantify enzymes and metabolic intermediates of the Escherichia coli fatty acid and phospholipid synthesis pathways, to describe how this organism measures temperature and restores optimal membrane fluidity within a single generation after a temperature shock. A first element of this regulatory system is a temperature-sensitive metabolic valve that allocates flux between the saturated and unsaturated fatty acid synthesis pathways via the branchpoint enzymes FabI and FabB. A second element is a transcription-based negative feedback loop that counteracts the temperature-sensitive valve. The combination of these elements accelerates membrane adaptation by causing a transient overshoot in the synthesis of saturated or unsaturated fatty acids following temperature shocks. This strategy is comparable to increasing the temperature of a water bath by adding water that is excessively hot rather than adding water at the desired temperature. These properties are captured in a mathematical model, which we use to show how hard-wired parameters calibrate the system to generate membrane compositions that maintain constant fluidity across temperatures. We hypothesize that core features of the E. coli system will prove to be ubiquitous features of homeoviscous adaptation systems.https://doi.org/10.1038/s41467-024-53677-5 |
| spellingShingle | Loles Hoogerland Stefan Pieter Hendrik van den Berg Yixing Suo Yuta W. Moriuchi Adja Zoumaro-Djayoon Esther Geurken Flora Yang Frank Bruggeman Michael D. Burkart Gregory Bokinsky A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli Nature Communications |
| title | A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli |
| title_full | A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli |
| title_fullStr | A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli |
| title_full_unstemmed | A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli |
| title_short | A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli |
| title_sort | temperature sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in escherichia coli |
| url | https://doi.org/10.1038/s41467-024-53677-5 |
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