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
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1038/s41396-021-00933-x

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.