A Postgenomic Appraisal of Osmotolerance in Listeria monocytogenes

Abstract

A characteristic feature of the intracellular food-borne pathogen Listeria monocytogenes is its ability to survive and even proliferate under a variety of hostile environmental conditions, particularly elevated osmolarity (10% NaCl) (47) and reduced temperature (Ϫ0.1°C) (75). Early physiological analysis revealed that this adaptation results, at least in part, from the accumulation of a restricted range of low-molecular-weight molecules termed osmolytes, or compatible solutes, owing to their compatibility with vital cellular processes at high internal concentrations (reviewed in reference 59). Initially restricted to betaine, carnitine, and proline (or proline-containing peptides), the list of compatible solutes promoting both salt and chill tolerances in Listeria has since been extended to include proline betaine, acetylcarnitine, gamma-butyrobetaine, and 3-dimethylsulfoniopropionate (6).Following the elegant biochemical and physiological analyses of the early 1990s, the listerial salt and chill stress response has recently become the focus of intense genetic analysis. A variety of innovative and imaginative molecular techniques led to the identification and subsequent characterization of some of the major genetic elements governing compatible-solute accumulation in Listeria. The recent publication of the listerial genome allows us for the first time to place the earlier experimentally generated data against the background of the in silico-based complete gene set. This exercise permits an informed overview of the complex interplay of systems controlling and enacting the listerial osmo-and cryostress responses.Beginning with a brief overview of the general principles underlying the biophysics of compatible-solute function, we review the development of our understanding of the mechanisms of compatible-solute accumulation in Listeria and use this information to attempt to construct a simplified model incorporating the known salt and chill stress response mechanisms of this ubiquitous and tenacious food-borne pathogen (Fig. 1.) In addition, we examine potential regulatory mechanisms governing osmolyte acquisition and suggest possible future directions in the field of listerial osmo-and cryotolerance. BACTERIAL OSMOADAPTATIONOsmoadaptation includes both the genetic and physiological manifestations of adaptation to low-water environments (26). In principle, two strategies of osmoadaptation have evolved to cope with life at elevated osmolarity (27): (i) the salt-in-cytoplasm type, restricted mainly to members of the family Halobacteriaceae (for a review, see reference 26), and (ii) the organic-osmolyte type, an adaptation strategy which has as its hallmarks a minimal requirement for genetic change and a high degree of flexibility in allowing organisms to cope with fluctuations in external osmolarity (77). The organic-osmolyte solution is a biphasic response in which increased levels of K ϩ (and its counterion, glutamate) represent the primary response, followed by a dramatic increase in the cytoplasmic concentrations ...

Antibiotic Susceptibility Profiles of Listeria monocytogenes Strains Isolated from Food Products and Clinical Samples

“…L. monocytogenes is a Gram-positive rod, capable of growing in conditions such as low temperature, acidic pH, high salt concentration, resistant to the procedures applied in the food industry to inactivate pathogenic microorganisms (3,4).…”

Cardiolipin Controls the Osmotic Stress Response and the Subcellular Location of Transporter ProP in Escherichia coli

“…These compounds are also called osmoprotectants because, when provided exogenously, they stimulate bacterial growth in high (but not low) osmotic pressure media. Well characterized, functionally redundant transporters, enzymes, and channels modulate the osmolyte composition of Gram-negative bacterium Escherichia coli (3)(4)(5). We are exploiting that system to learn how osmotic pressure is sensed, how resulting signals are transduced, and how cells respond by modulating their own structure, growth, and division.…”

Cronobacter sakazakii: stress survival and virulence potential in an opportunistic foodborne pathogen

“…62 One of the most extensively studied Gram-positive foodborne pathogens in this respect is L. monocytogenes. 57 This pathogen uses the compatible solutes glycine betaine, 63 proline 64 and carnitine 65 to counteract the cytotoxic effects of elevated osmolality. Indeed, Gram-negative bacteria share similar preferences and mechanisms of compatible solute accumulation as those seen in Gram-positives.…”

“…44 Further elucidation of C. sakazakii osmotolerance is aided by the wealth of knowledge available on how other bacterial cells overcome hyperosmotic stress and it is believed that C. sakazakii responds in a similar way. [55][56][57] Bacterial cells in general need to maintain an intracellular osmotic pressure greater than that of the surrounding media in order to generate cell turgor and prevent plasmolysis and ultimately cell death. 58 Most bacteria survive osmotic stress through a biphasic response, which first involves the accumulation of potassium and its counter ion glutamate; representing the primary response.…”