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The ability of Listeria monocytogenes to adapt to low temperature, low pH, and osmotic stress, to withstand cleaning and disinfection agents, to induce stress-related cross-protection responses, and to form biofilms, enables it to prevail and survive most of the common safety measures employed in industrial-scale food processing to ensure food safety. The objective of this study was to determine the changes that occur in the lipid composition of the membrane of L. monocytogenes under the conditions of the manufacture and storage of a laboratory-prepared soft cheese (feta type). The results show that L. monocytogenes cells present in the raw milk may survive the cheese manufacturing process as well as the storage period and that the history of the inoculated cells has an effect on their behavior during storage of the cheese. The bacterium seems to follow different pathways and adopt different strategies to preserve the optimal fluidity and functions of the membrane depending on the length of storage time and the history of the inoculated cells. In this context, cells derived from pre-inoculated cells grown in optimal or acidic conditions showed an increase in the number of straight chain fatty acids (SCFA) relative to branched ones (BCFA), without altering the ratio of BCFA C15:0 to BCFA C17:0 and the ratio of iso to anteiso FA. Alternatively, those cells derived from pre-inoculated cells grown in presence of benzalkonium chloride followed a different pathway. These cells achieved a balance between optimal fluidity and solid phase membrane not only by changes in SCFA content, but also by changes in the ratios of BCFA C15:0 to C17:0 and of iso to anteiso fatty acids. This latter approach to maintain membrane fluidity seems to be paired with the different survival trends of the bacterium under the conditions of this study.