Staphylococcus aureus Carotenoids Modulate the Thermotropic Phase Behavior of Model Systems That Mimic Its Membrane Composition

Abstract

Staphylococcus aureus (S. aureus) is a pathogenic gram-positive bacterium that normally resides in the skin and nose of the human body. It is subject to fluctuations in environmental conditions that may affect the integrity of the membrane. S. aureus produces carotenoids, which act as antioxidants. However, these carotenoids have also been implicated in modulating the biophysical properties of the membrane. Here, we investigate how carotenoids modulate the thermotropic phase behavior of model systems that mimic the phospholipid composition of S. aureus. We found that carotenoids depress the main phase transition of DMPG and CL, indicating that they strongly affect cooperativity of membrane lipids in their gel phase. In addition, carotenoids modulate the phase behavior of mixtures of DMPG and CL, indicating that they may play a role in modulation of lipid domain formation in S. aureus membranes.

Involvement of Versatile Bacteria Belonging to the Genus Arthrobacter in Milk and Dairy Products

“…In addition, these compounds were reported to engage in photoprotection, and membrane stabilization [ 56 , 57 , 58 ]. Certain studies report that carotenoids possibly lowered the phase transition temperature of synthetic lipids and worked as regulators for membrane fluidity since they showed an important role in the causative function in the modulation of membrane parameters [ 59 , 60 ]. It was found that carotenoids increased membrane order with concurrent maintenance of lateral lipid motility, which resulted in a liquid-ordered membrane state [ 61 ] The increase in membrane order was indicated to be related to a simultaneous increase in membrane fluidity, and an increase in the concentration of carotenoids led to an increase in the resistance of the cell against freeze-thaw stress [ 54 ].…”

Staphylococcus aureus Modulates Carotenoid and Phospholipid Content in Response to Oxygen-Restricted Growth Conditions, Triggering Changes in Membrane Biophysical Properties

“…The physical aspects that were explored were lipid headgroup spacing as measured with Laurdan fluorescence GP, mobility in the membrane core as measured with DPH fluorescence anisotropy, and lipid acyl chain order as measured with FTIR spectroscopy. Thermotropic measurements were performed in order to observe the behavior of the membrane in the gel phase regime at low temperatures and the liquid-crystalline regime at high temperatures, and also to assess gel to liquid-crystalline phase transition temperatures, which are important indicators of the membrane physical state [6,8,10,11]. Downward shifts in the phase transition temperature indicate that the liquid-crystalline phase of the membrane is stabilized with respect to the gel phase.…”

“…This result is important due to the fact that the more disordered liquid-crystalline phase is considered the physiologically relevant phase due to its increased mobility. By making the gel phase more disordered, carotenoid production may help the bacteria maintain a physiologically active membrane at low temperatures [8,10]. A recent study by Seel et al showed that carotenoids regulate membrane fluidity in Staphylococcus xylosus, in particular greatly affecting the fluidity of the membrane at low temperatures [32].…”

“…aureus has evolved the ability to modify the lipid composition of its membranes in response to environmental stresses such as oxidative stress, osmotic stress, and the presence of antimicrobial agents [5][6][7][8], as well as during changes in S. aureus growth conditions [6,8]. Modifications in phospholipid headgroup and acyl chain composition or carotenoid content influence the biophysical properties of S. aureus membranes [6,9], leading to changes in membrane rigidity and lipid packing [6,8,10,11].…”

“…Due to a series of conjugated double bonds, the rigid structure of the diaponeurosporenoic acid leads to increased membrane rigidity, which confers on S. aureus a higher resistance to antimicrobial peptides [15]. This is in addition to its protective role as a free radical scavenger [8,13,[16][17][18] The main phospholipid components in S. aureus membranes are the anionic phospholipids phosphatidyl-glycerol (PG) and cardiolipin (CL), as well as the cationic phospholipid lysyl-phosphatidylglycerol (Lys-PG), which are present in the membrane with varying acyl chain lengths [6,10,19]. Phospholipid acyl chains are mainly saturated or branched in isoand anteisoconformations, where the branched/saturated ratio helps modulate the level of lipid packing in the membrane [6,20].…”