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Aminolipids elicit functional trade-offs between competitiveness and bacteriophage attachment in Ruegeria pomeroyi

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Stirrup, Rachel, Mausz, Michaela A., Silvano, Eleonora, Murphy, Andrew, Guillonneau, Richard, Quareshy, Mussa, Rihtman, Branko, Aguilo Ferretjans, Maria, He, Ruo, Todd, Jonathan D., Chen, Feng, Scanlan, David J. and Chen, Yin (2023) Aminolipids elicit functional trade-offs between competitiveness and bacteriophage attachment in Ruegeria pomeroyi. ISME Journal, 17 (3). pp. 315-325. doi:10.1038/s41396-022-01346-0 ISSN 1751-7362.

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Official URL: https://doi.org/10.1038/s41396-022-01346-0

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Abstract

Lipids play a crucial role in maintaining cell integrity and homeostasis with the surrounding environment. Cosmopolitan marine roseobacter clade (MRC) and SAR11 clade bacteria are unique in that, in addition to glycerophospholipids, they also produce an array of amino acid-containing lipids that are conjugated with beta-hydroxy fatty acids through an amide bond. Two of these aminolipids, the ornithine aminolipid (OL) and the glutamine aminolipid (QL), are synthesized using the O-acetyltransferase OlsA. Here, we demonstrate that OL and QL are present in both the inner and outer membranes of the Gram-negative MRC bacterium Ruegeria pomeroyi DSS-3. In an olsA mutant, loss of these aminolipids is compensated by a concurrent increase in glycerophospholipids. The inability to produce aminolipids caused significant changes in the membrane proteome, with the membrane being less permeable and key nutrient transporters being downregulated while proteins involved in the membrane stress response were upregulated. Indeed, the import of 14C-labelled choline and dimethylsulfoniopropionate, as a proxy for the transport of key marine nutrients across membranes, was significantly impaired in the olsA mutant. Moreover, the olsA mutant was significantly less competitive than the wild type (WT) being unable to compete with the WT strain in co-culture. However, the olsA mutant unable to synthesize these aminolipids is less susceptible to phage attachment. Together, these data reveal a critical role for aminolipids in the ecophysiology of this important clade of marine bacteria and a trade-off between growth and avoidance of bacteriophage attachment.

Item Type: Journal Article
Alternative Title:
Subjects: Q Science > QP Physiology
Q Science > QR Microbiology
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Lipids, Microbial lipids, Bacteria -- Physiology, Marine bacteria, Heterotrophic bacteria, Bacteriophages
Journal or Publication Title: ISME Journal
Publisher: Nature Publishing Group
ISSN: 1751-7362
Official Date: March 2023
Dates:
DateEvent
March 2023Published
7 December 2022Available
21 November 2022Accepted
Volume: 17
Number: 3
Page Range: pp. 315-325
DOI: 10.1038/s41396-022-01346-0
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access (Creative Commons)
Date of first compliant deposit: 22 November 2022
Date of first compliant Open Access: 14 December 2022
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
726116Horizon 2020 Framework Programmehttp://dx.doi.org/10.13039/100010661
NE/M002233/1[NERC] Natural Environment Research Councilhttp://dx.doi.org/10.13039/501100000270
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