A novel class of sulfur-containing aminolipids widespread in marine roseobacters

• Published in: The ISME Journal Vol. 15; no. 8; pp. 2440 - 2453
• Main Authors: Smith, Alastair F., Silvano, Eleonora, Päuker, Orsola, Guillonneau, Richard, Quareshy, Mussa, Murphy, Andrew, Mausz, Michaela A., Stirrup, Rachel, Rihtman, Branko, Aguilo-Ferretjans, Maria, Brandsma, Joost, Petersen, Jörn, Scanlan, David J., Chen, Yin
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.08.2021; Oxford University Press
• Subjects: 631/326; 631/337; Acyltransferase; Amino acids; Bacteria; Biofilms; Biomedical and Life Sciences; Biosynthesis; Ecology; Environmental changes; Evolutionary Biology; Glutamine; Life Sciences; Lipid composition; Lipids; Lysophosphatidic acid; Marine ecosystems; Mass spectrometry; Mass spectroscopy; Membranes; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Oceans; Ornithine; Phosphatidic acid; Phospholipids; Phosphorus; Sequence analysis; Sulfur; Transposon mutagenesis
• DOI: 10.1038/s41396-021-00933-x
• ISSN: 1751-7362; 1751-7370

Marine roseobacter group bacteria are numerically abundant and ecologically important players in ocean ecosystems. These bacteria are capable of modifying their membrane lipid composition in response to environmental change. Remarkably, a variety of lipids are produced in these bacteria, including phosphorus-containing glycerophospholipids and several amino acid-containing aminolipids such as ornithine lipids and glutamine lipids. Here, we present the identification and characterization of a novel sulfur-containing aminolipid (SAL) in roseobacters. Using high resolution accurate mass spectrometry, a SAL was found in the lipid extract of Ruegeria pomeroyi DSS-3 and Phaeobacter inhibens DSM 17395. Using comparative genomics, transposon mutagenesis and targeted gene knockout, we identified a gene encoding a putative lyso-lipid acyltransferase, designated salA , which is essential for the biosynthesis of this SAL. Multiple sequence analysis and structural modeling suggest that SalA is a novel member of the lysophosphatidic acid acyltransferase (LPAAT) family, the prototype of which is the PlsC acyltransferase responsible for the biosynthesis of the phospholipid phosphatidic acid. SAL appears to play a key role in biofilm formation in roseobacters. salA is widely distributed in Tara Oceans metagenomes and actively expressed in Tara Oceans metatranscriptomes. Our results raise the importance of sulfur-containing membrane aminolipids in marine bacteria.