Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants
Abstract Background Many organisms rely on mineral nutrients taken directly from the soil or aquatic environment, and therefore, developed mechanisms to cope with the limitation of a given essential nutrient. For example, photosynthetic cells have well-defined responses to phosphate limitation, incl...
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| Format: | Article |
| Language: | English |
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BMC
2023-11-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01775-z |
| _version_ | 1797413989688279040 |
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| author | Stéphanie Bolik Alexander Schlaich Tetiana Mukhina Alberto Amato Olivier Bastien Emanuel Schneck Bruno Demé Juliette Jouhet |
| author_facet | Stéphanie Bolik Alexander Schlaich Tetiana Mukhina Alberto Amato Olivier Bastien Emanuel Schneck Bruno Demé Juliette Jouhet |
| author_sort | Stéphanie Bolik |
| collection | DOAJ |
| description | Abstract Background Many organisms rely on mineral nutrients taken directly from the soil or aquatic environment, and therefore, developed mechanisms to cope with the limitation of a given essential nutrient. For example, photosynthetic cells have well-defined responses to phosphate limitation, including the replacement of cellular membrane phospholipids with non-phosphorous lipids. Under phosphate starvation, phospholipids in extraplastidial membranes are replaced by betaine lipids in microalgae. In higher plants, the synthesis of betaine lipid is lost, driving plants to other strategies to cope with phosphate starvation where they replace their phospholipids by glycolipids. Results The aim of this work was to evaluate to what extent betaine lipids and PC lipids share physicochemical properties and could substitute for each other. By neutron diffraction experiments and dynamic molecular simulation of two synthetic lipids, the dipalmitoylphosphatidylcholine (DPPC) and the dipalmitoyl-diacylglyceryl-N,N,N-trimethylhomoserine (DP-DGTS), we found that DP-DGTS bilayers are thicker than DPPC bilayers and therefore are more rigid. Furthermore, DP-DGTS bilayers are more repulsive, especially at long range, maybe due to unexpected unscreened electrostatic contribution. Finally, DP-DGTS bilayers could coexist in the gel and fluid phases. Conclusion The different properties and hydration responses of PC and DGTS provide an explanation for the diversity of betaine lipids observed in marine organisms and for their disappearance in seed plants. |
| first_indexed | 2024-03-09T05:26:33Z |
| format | Article |
| id | doaj.art-b07fb596b69a41058e2aad97dc88665c |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-09T05:26:33Z |
| publishDate | 2023-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-b07fb596b69a41058e2aad97dc88665c2023-12-03T12:36:27ZengBMCBMC Biology1741-70072023-11-0121111610.1186/s12915-023-01775-zLipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plantsStéphanie Bolik0Alexander Schlaich1Tetiana Mukhina2Alberto Amato3Olivier Bastien4Emanuel Schneck5Bruno Demé6Juliette Jouhet7Laboratoire Physiologie Cellulaire Et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIGInstitute for Computational Physics, Universität StuttgartInstitute for Condensed Matter PhysicsLaboratoire Physiologie Cellulaire Et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIGLaboratoire Physiologie Cellulaire Et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIGInstitute for Condensed Matter PhysicsLarge Scale Structures Group, Institut Laue-LangevinLaboratoire Physiologie Cellulaire Et Végétale, Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIGAbstract Background Many organisms rely on mineral nutrients taken directly from the soil or aquatic environment, and therefore, developed mechanisms to cope with the limitation of a given essential nutrient. For example, photosynthetic cells have well-defined responses to phosphate limitation, including the replacement of cellular membrane phospholipids with non-phosphorous lipids. Under phosphate starvation, phospholipids in extraplastidial membranes are replaced by betaine lipids in microalgae. In higher plants, the synthesis of betaine lipid is lost, driving plants to other strategies to cope with phosphate starvation where they replace their phospholipids by glycolipids. Results The aim of this work was to evaluate to what extent betaine lipids and PC lipids share physicochemical properties and could substitute for each other. By neutron diffraction experiments and dynamic molecular simulation of two synthetic lipids, the dipalmitoylphosphatidylcholine (DPPC) and the dipalmitoyl-diacylglyceryl-N,N,N-trimethylhomoserine (DP-DGTS), we found that DP-DGTS bilayers are thicker than DPPC bilayers and therefore are more rigid. Furthermore, DP-DGTS bilayers are more repulsive, especially at long range, maybe due to unexpected unscreened electrostatic contribution. Finally, DP-DGTS bilayers could coexist in the gel and fluid phases. Conclusion The different properties and hydration responses of PC and DGTS provide an explanation for the diversity of betaine lipids observed in marine organisms and for their disappearance in seed plants.https://doi.org/10.1186/s12915-023-01775-zBetaine lipidNeutron membrane diffractionMolecular dynamicsPhosphate starvationAlgaeEvolution |
| spellingShingle | Stéphanie Bolik Alexander Schlaich Tetiana Mukhina Alberto Amato Olivier Bastien Emanuel Schneck Bruno Demé Juliette Jouhet Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants BMC Biology Betaine lipid Neutron membrane diffraction Molecular dynamics Phosphate starvation Algae Evolution |
| title | Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants |
| title_full | Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants |
| title_fullStr | Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants |
| title_full_unstemmed | Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants |
| title_short | Lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants |
| title_sort | lipid bilayer properties potentially contributed to the evolutionary disappearance of betaine lipids in seed plants |
| topic | Betaine lipid Neutron membrane diffraction Molecular dynamics Phosphate starvation Algae Evolution |
| url | https://doi.org/10.1186/s12915-023-01775-z |
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