Enhancement of low-temperature growth of <i>Staphylococcus aureus</i> by low concentrations of antimicrobial unsaturated fatty acids

It is well established that <i>Staphylococcus aureus</i> can incorporate straight-chain unsaturated fatty acids (SCUFAs) into its lipids in addition to the normally biosynthesized branched-chain and straight-chain saturated fatty acids. Incorporation of oleic acid into <i>S. aureus</i> lipids has recently been shown to significantly enhance <i>S. aureus</i> growth at low temperatures due to the greater fluidity imparted to the membrane. Here, we show that low-temperature growth of <i>S. aureus</i> is not limited to oleic acid but enhanced also by various antimicrobial SCUFAs when present at low concentrations. A <i>fakA</i>-deficient strain did not show SCUFA-induced growth stimulation, which indicates that the fatty acid kinase is necessary for SCUFA incorporation into membrane lipids to promote low-temperature growth. Determination of total lipid fatty acid composition showed that incorporated SCUFAs make up ~12% or less of the total fatty acids. Lipidomic investigations revealed elevated synthesis of diglucosyldiglyceride in the absence or presence of SCUFAs. SCUFAs were incorporated into diglucosyldiglyceride to a greater extent than phosphatidyglycerol at both 12 °C and 37 °C. The presence of SCUFAs at low temperatures also enhanced production of the carotenoid staphyloxanthin. The results suggest that multiple strategies are at play in the membrane adaptation of <i>S. aureus</i> to low temperatures. Inclusion of oleic acid in media decreased the minimum growth temperature of <i>S. aureus</i>, suggesting that the presence of SCUFAs in food may facilitate the growth of <i>S. aureus</i> at low temperature. Also, incorporation of SCUFAs into lipids may promote the disruption of the membrane by SCUFAs.