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Lipidomics of Thalassiosira pseudonana under phosphorus stress reveal underlying phospholipid substitution dynamics and novel diglycosylceramide substitutes

Lipidomics of Thalassiosira pseudonana under phosphorus stress reveal underlying phospholipid substitution dynamics and novel diglycosylceramide substitutes
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 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.
0099-2240
Hunter, J.E.
13561242-07d5-47ba-8217-774706f4e5ce
Brandsma, Joost
b4c553dc-9444-466a-b352-25fd8fa25ee7
Dymond, Marcus K.
e180765b-039e-47ff-9841-ce6a5123a519
Koster, Grielof
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Moore, C. Mark
7ec80b7b-bedc-4dd5-8924-0f5d01927b12
Postle, Anthony
0fa17988-b4a0-4cdc-819a-9ae15c5dad66
Mills, Rachel
a664f299-1a34-4b63-9988-1e599b756706
Attard, George S.
3219075d-2364-4f00-aeb9-1d90f8cd0d36
Hunter, J.E.
13561242-07d5-47ba-8217-774706f4e5ce
Brandsma, Joost
b4c553dc-9444-466a-b352-25fd8fa25ee7
Dymond, Marcus K.
e180765b-039e-47ff-9841-ce6a5123a519
Koster, Grielof
e404c38a-6f48-430a-adf0-5208228cb9e7
Moore, C. Mark
7ec80b7b-bedc-4dd5-8924-0f5d01927b12
Postle, Anthony
0fa17988-b4a0-4cdc-819a-9ae15c5dad66
Mills, Rachel
a664f299-1a34-4b63-9988-1e599b756706
Attard, George S.
3219075d-2364-4f00-aeb9-1d90f8cd0d36

Hunter, J.E., Brandsma, Joost, Dymond, Marcus K., Koster, Grielof, Moore, C. Mark, Postle, Anthony, Mills, Rachel and Attard, George S. (2018) Lipidomics of Thalassiosira pseudonana under phosphorus stress reveal underlying phospholipid substitution dynamics and novel diglycosylceramide substitutes. Applied and Environmental Microbiology, 84 (6), [e02034-17]. (doi:10.1128/AEM.02034-17).

Record type: Article

Abstract

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.

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AEM.02034-17.full - Accepted Manuscript
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Accepted/In Press date: 21 December 2017
e-pub ahead of print date: 5 January 2018
Published date: March 2018

Identifiers

Local EPrints ID: 418137
URI: http://eprints.soton.ac.uk/id/eprint/418137
ISSN: 0099-2240
PURE UUID: cc3e17e7-8b66-487d-81e2-764dc8e41bb1
ORCID for Anthony Postle: ORCID iD orcid.org/0000-0001-7361-0756
ORCID for Rachel Mills: ORCID iD orcid.org/0000-0002-9811-246X
ORCID for George S. Attard: ORCID iD orcid.org/0000-0001-8304-0742

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Date deposited: 22 Feb 2018 17:30
Last modified: 18 Feb 2021 16:42

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Contributors

Author: J.E. Hunter
Author: Joost Brandsma
Author: Marcus K. Dymond
Author: Grielof Koster
Author: C. Mark Moore
Author: Anthony Postle ORCID iD
Author: Rachel Mills ORCID iD

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