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Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes
Phytoplankton replace phosphorus-containing lipids (P-lipids) with non-P analogues, boosting growth in P-limited oceans. In the model diatom Thalassiosira pseudonana, the substitution dynamics of lipid headgroups are well described, but those of the individual lipids, differing in fatty acid composi...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5835749/ https://www.ncbi.nlm.nih.gov/pubmed/29305510 http://dx.doi.org/10.1128/AEM.02034-17 |
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author | Hunter, Jonathan E. Brandsma, Joost Dymond, Marcus K. Koster, Grielof Moore, C. Mark Postle, Anthony D. Mills, Rachel A. Attard, George S. |
author_facet | Hunter, Jonathan E. Brandsma, Joost Dymond, Marcus K. Koster, Grielof Moore, C. Mark Postle, Anthony D. Mills, Rachel A. Attard, George S. |
author_sort | Hunter, Jonathan E. |
collection | PubMed |
description | Phytoplankton replace phosphorus-containing lipids (P-lipids) with non-P analogues, boosting growth in P-limited oceans. In the model diatom Thalassiosira pseudonana, the substitution dynamics of lipid headgroups are well described, but those of the individual lipids, differing in fatty acid composition, are unknown. Moreover, the behavior of lipids outside the common headgroup classes and the relationship between lipid substitution and cellular particulate organic P (POP) have yet to be reported. We investigated these through the mass spectrometric lipidomics of P-replete (P(+)) and P-depleted (P(−)) T. pseudonana cultures. Nonlipidic POP was depleted rapidly by the initiation of P stress, followed by the cessation of P-lipid biosynthesis and per-cell reductions in the P-lipid levels of successive generations. Minor P-lipid degradative breakdown was observed, releasing P for other processes, but most P-lipids remained intact. This may confer an advantage on efficient heterotrophic lipid consumers in P-limited oceans. Glycerophosphatidylcholine (PC), the predominant P-lipid, was similar in composition to its betaine substitute lipid. During substitution, PC was less abundant per cell and was more highly unsaturated in composition. This may reflect underlying biosynthetic processes or the regulation of membrane biophysical properties subject to lipid substitution. Finally, levels of several diglycosylceramide lipids increased as much as 10-fold under P stress. These represent novel substitute lipids and potential biomarkers for the study of P limitation in situ, contributing to growing evidence highlighting the importance of sphingolipids in phycology. These findings contribute much to our understanding of P-lipid substitution, a powerful and widespread adaptation to P limitation in the oligotrophic ocean. IMPORTANCE Unicellular organisms replace phosphorus (P)-containing membrane lipids with non-P substitutes when P is scarce, allowing greater growth of populations. Previous research with the model diatom species Thalassiosira pseudonana grouped lipids by polar headgroups in their chemical structures. The significance of the research reported here is threefold. (i) We described the individual lipids within the headgroups during P-lipid substitution, revealing the relationships between lipid headgroups and hinting at the underlying biochemical processes. (ii) We measured total cellular P, placing P-lipid substitution in the context of the broader response to P stress and yielding insight into the implications of substitution in the marine environment. (iii) We identified lipids previously unknown in this system, revealing a new type of non-P substitute lipid, which is potentially useful as a biomarker for the investigation of P limitation in the ocean. |
format | Online Article Text |
id | pubmed-5835749 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-58357492018-03-29 Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes Hunter, Jonathan E. Brandsma, Joost Dymond, Marcus K. Koster, Grielof Moore, C. Mark Postle, Anthony D. Mills, Rachel A. Attard, George S. Appl Environ Microbiol Physiology Phytoplankton replace phosphorus-containing lipids (P-lipids) with non-P analogues, boosting growth in P-limited oceans. In the model diatom Thalassiosira pseudonana, the substitution dynamics of lipid headgroups are well described, but those of the individual lipids, differing in fatty acid composition, are unknown. Moreover, the behavior of lipids outside the common headgroup classes and the relationship between lipid substitution and cellular particulate organic P (POP) have yet to be reported. We investigated these through the mass spectrometric lipidomics of P-replete (P(+)) and P-depleted (P(−)) T. pseudonana cultures. Nonlipidic POP was depleted rapidly by the initiation of P stress, followed by the cessation of P-lipid biosynthesis and per-cell reductions in the P-lipid levels of successive generations. Minor P-lipid degradative breakdown was observed, releasing P for other processes, but most P-lipids remained intact. This may confer an advantage on efficient heterotrophic lipid consumers in P-limited oceans. Glycerophosphatidylcholine (PC), the predominant P-lipid, was similar in composition to its betaine substitute lipid. During substitution, PC was less abundant per cell and was more highly unsaturated in composition. This may reflect underlying biosynthetic processes or the regulation of membrane biophysical properties subject to lipid substitution. Finally, levels of several diglycosylceramide lipids increased as much as 10-fold under P stress. These represent novel substitute lipids and potential biomarkers for the study of P limitation in situ, contributing to growing evidence highlighting the importance of sphingolipids in phycology. These findings contribute much to our understanding of P-lipid substitution, a powerful and widespread adaptation to P limitation in the oligotrophic ocean. IMPORTANCE Unicellular organisms replace phosphorus (P)-containing membrane lipids with non-P substitutes when P is scarce, allowing greater growth of populations. Previous research with the model diatom species Thalassiosira pseudonana grouped lipids by polar headgroups in their chemical structures. The significance of the research reported here is threefold. (i) We described the individual lipids within the headgroups during P-lipid substitution, revealing the relationships between lipid headgroups and hinting at the underlying biochemical processes. (ii) We measured total cellular P, placing P-lipid substitution in the context of the broader response to P stress and yielding insight into the implications of substitution in the marine environment. (iii) We identified lipids previously unknown in this system, revealing a new type of non-P substitute lipid, which is potentially useful as a biomarker for the investigation of P limitation in the ocean. American Society for Microbiology 2018-03-01 /pmc/articles/PMC5835749/ /pubmed/29305510 http://dx.doi.org/10.1128/AEM.02034-17 Text en Copyright © 2018 Hunter et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Physiology Hunter, Jonathan E. Brandsma, Joost Dymond, Marcus K. Koster, Grielof Moore, C. Mark Postle, Anthony D. Mills, Rachel A. Attard, George S. Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes |
title | Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes |
title_full | Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes |
title_fullStr | Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes |
title_full_unstemmed | Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes |
title_short | Lipidomics of Thalassiosira pseudonana under Phosphorus Stress Reveal Underlying Phospholipid Substitution Dynamics and Novel Diglycosylceramide Substitutes |
title_sort | lipidomics of thalassiosira pseudonana under phosphorus stress reveal underlying phospholipid substitution dynamics and novel diglycosylceramide substitutes |
topic | Physiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5835749/ https://www.ncbi.nlm.nih.gov/pubmed/29305510 http://dx.doi.org/10.1128/AEM.02034-17 |
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