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Elucidation of glutamine lipid biosynthesis in marine bacteria reveals its importance under phosphorus deplete growth in Rhodobacteraceae
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Smith, Alastair, Rihtman, Branko, Stirrup, Rachel, Silvano, Eleonora, Mausz, Michaela A., Scanlan, David J. and Chen, Yin (2019) Elucidation of glutamine lipid biosynthesis in marine bacteria reveals its importance under phosphorus deplete growth in Rhodobacteraceae. The ISME Journal, 13 . pp. 39-49. doi:10.1038/s41396-018-0249-z ISSN 1751-7362.
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Official URL: https://doi.org/10.1038/s41396-018-0249-z
Abstract
Marine microorganisms employ multiple strategies to cope with transient and persistent nutrient limitation, one of which, for alleviating phosphorus (P) stress, is to substitute membrane glycerophospholipids with non-P containing surrogate lipids. Such a membrane lipid remodelling strategy enables the most abundant marine phytoplankton and heterotrophic bacteria to adapt successfully to nutrient scarcity in marine surface waters. An important group of non-P lipids, the aminolipids which lack a diacylglycerol backbone, are poorly studied in marine microbes. Here, using a combination of genetic, lipidomics and metagenomics approaches, we reveal for the first time the genes (glsB, olsA) required for the formation of the glutamine-containing aminolipid. Construction of a knockout mutant in either glsB or olsA in the model marine bacterium Ruegeria pomeroyi DSS-3 completely abolished glutamine lipid production. Moreover, both mutants showed a considerable growth cost under P-deplete conditions and the olsA mutant, that is unable to produce the glutamine and ornithine aminolipids, ceased to grow under P-deplete conditions. Analysis of sequenced microbial genomes show that glsB is primarily confined to the Rhodobacteraceae family, which includes the ecologically important marine Roseobacter clade that are key players in the marine sulphur and nitrogen cycles. Analysis of the genes involved in glutamine lipid biosynthesis in the Tara ocean metagenome dataset revealed the global occurrence of glsB in marine surface waters and a positive correlation between glsB abundance and N* (a measure of the deviation from the canonical Redfield ratio), suggesting glutamine lipid plays an important role in the adaptation of marine Rhodobacteraceae to P limitation.
| Item Type: | Journal Article | |||||||||
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| Subjects: | Q Science > QK Botany Q Science > QR Microbiology |
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| Divisions: | Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- ) | |||||||||
| Library of Congress Subject Headings (LCSH): | Phytoplankton, Heterotrophic bacteria, Lipids, Glutamine, Biosynthesis, Phosphorus | |||||||||
| Journal or Publication Title: | The ISME Journal | |||||||||
| Publisher: | Nature Publishing Group | |||||||||
| ISSN: | 1751-7362 | |||||||||
| Official Date: | January 2019 | |||||||||
| Dates: |
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| Volume: | 13 | |||||||||
| Page Range: | pp. 39-49 | |||||||||
| DOI: | 10.1038/s41396-018-0249-z | |||||||||
| Status: | Peer Reviewed | |||||||||
| Publication Status: | Published | |||||||||
| Access rights to Published version: | Open Access (Creative Commons) | |||||||||
| Date of first compliant deposit: | 17 July 2018 | |||||||||
| Date of first compliant Open Access: | 8 October 2018 | |||||||||
| RIOXX Funder/Project Grant: |
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