Evidence for feedback (trans) regulation of, and two systems for, glycine betaine transport by Staphylococcus aureus

Stimeling, Kurt W.; Graham, James E.; Kaenjak, Anisa; Wilkinson, Brian J.

doi:10.1099/13500872-140-11-3139

Cited by 30 publications

(20 citation statements)

References 11 publications

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“…These data may explain why Patchett et al (21) observed much lower betaine uptake rates in L. monocytogenes NCTC 7973 (5 to 10 times lower) than we did in L. monocytogenes Scott A. Their studies were conducted with washed cells following growth in broth, which is known to contain significant amounts of betaine and carnitine (14,15,22,25,27). Accumulation of these compatible solutes during growth could have resulted in the reduced uptake rates for betaine.…”

Section: Figmentioning

confidence: 62%

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Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals

et al. 1997

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The naturally occurring compatible solutes betaine and L-carnitine allow the food-borne pathogen Listeria monocytogenes to adjust to environments of high osmotic strength. Previously, it was demonstrated that L. monocytogenes possesses an ATP-dependent L-carnitine transporter (A. Verheul, F. M. Rombouts, R. R. Beumer, and T. Abee, J. Bacteriol. 177:3205-3212, 1995). The present study reveals that betaine and L-carnitine are taken up by separate highly specific transport systems and support a secondary transport mechanism for betaine uptake in L. monocytogenes. The initial uptake rates of betaine and L-carnitine are not influenced by an osmotic upshock, but the duration of transport of both osmolytes is directly related to the osmotic strength of the medium. Regulation of uptake of both betaine and L-carnitine is subject to inhibition by preaccumulated solute. Internal betaine inhibits not only transport of external betaine but also that of L-carnitine and, similarly, internal L-carnitine inhibits transport of both betaine and L-carnitine. The inhibition is alleviated upon osmotic upshock, which suggests that alterations in membrane structure are transmitted to the allosteric binding sites for betaine and L-carnitine of both transporters at the inner surface of the membrane. Upon osmotic downshock, betaine and L-carnitine are rapidly released by L. monocytogenes as a consequence of activation of a channel-like activity. The osmolyte-sensing mechanism described is new and is consistent with various unexplained observations of osmoregulation in other bacteria.Food-borne listeriosis caused by Listeria monocytogenes has emerged as a topic of considerable public health concern over the past decade. The infection is encountered in neonates, elderly persons, pregnant women, and the immunocompromised, and symptoms may include sepsis, meningitis, infection of the central nervous system, abortion, and stillbirth, with fatality rates of approximately 25%. The ubiquitous distribution of L. monocytogenes in the environment and its relative high tolerance to environmental stresses such as low temperature and high osmotic strength contribute to its status as a hazard in minimally processed ready-to-eat refrigerated products (7).Cold and salt tolerance in L. monocytogenes can be imparted by betaine and L-carnitine. Betaine is present in high concentrations in foods originating from plants, whereas foods of animal origin generally have a high carnitine content (3,15,21,30). The osmoprotective capacity of betaine is well-known among prokaryotic organisms, whereas, so far, L-carnitine has been recognized only as an osmolyte in L. monocytogenes, Lactobacillus plantarum, and Escherichia coli (3,(12)(13)(14). The involvement of betaine and L-carnitine in cold tolerance of the psychrotroph L. monocytogenes has recently been reported (15,25,30). Uptake of L-carnitine in L. monocytogenes is mediated by a constitutively expressed transporter that is driven by ATP. Competition experiments revealed that the L-carnitine transporter has a hig...

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Section: Figmentioning

confidence: 62%

“…Accumulation of compatible solutes in the absence of osmotic stress has also been described for other gram-positive bacteria. This is thought to be a direct consequence of their maintenance of a relatively high turgor pressure compared to that of gram-negative bacteria (5,11,27,31).…”

Section: Figmentioning

confidence: 99%

Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals

et al. 1997

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“…In the present communication, we report the isolation of the betP gene encoding the glycine betaine transport system of C. glutamicum. Previously, only a low-affinity glycine betaine transport system in S. aureus which is regulated by a hyperosmotic shift was known; however, the gene encoding this protein is still unknown (26,30). The betP gene of C. glutamicum identified in this study is the first known gene encoding an osmotically stimulated secondary transport system in grampositive bacteria.…”

Section: Discussionmentioning

confidence: 85%

“…Also, Staphylococcus aureus accumulates glycine betaine and proline as major osmoprotectants (1). Two feedback-regulated proline uptake systems, a low-affinity one and a high-affinity one, were identified in this organism (26,30,31).…”

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confidence: 99%

Isolation, characterization, and expression of the Corynebacterium glutamicum betP gene, encoding the transport system for the compatible solute glycine betaine

1996

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Corynebacterium glutamicum accumulates glycine betaine under conditions of high osmolarity. Previous work revealed the existence of a high-affinity glycine betaine permease which is osmotically regulated. In the present study, the corresponding gene was cloned. The betP gene, encoding the glycine betaine uptake carrier, was isolated by heterologous complementation of mutant strain Escherichia coli MKH13. From sequence analysis it is predicted to encode a protein of 595 amino acids. This protein shares 36% identity with the choline transport system BetT and 28% identity with the carnitine transport system CaiT of E. coli, as well as 38% identity with a protein with an unknown function from Haemophilus influenzae. Analysis of hydropathy indicated a common structure for all four transport proteins. After heterologous expression of betP in E. coli MKH13, the measured K m values for glycine betaine and the cotransported Na ؉ were similar to those found in C. glutamicum, whereas the modulation of activity by osmotic gradients was shifted to lower osmotic values.

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“…The observed trans inhibition is alleviated upon osmotic upshock, which suggests that alterations in membrane structure are transmitted to the allosteric binding sites for betaine and carnitine of both transporters at the inner surface of the membrane. The linkage of the trans-inhibitory effect to the osmotic strength of the environment is also observed in Lactobacillus plantarum (53) and Staphylococcus aureus (54,69) and thus may form part of a general strategy to tune the intracellular osmolarity and maintain the cell turgor within certain limits.…”

Section: Regulationmentioning

confidence: 99%

A Postgenomic Appraisal of Osmotolerance in Listeria monocytogenes

Sleator

Gahan

Hill

2003

Appl Environ Microbiol

135

105

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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 ...

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Evidence for feedback (trans) regulation of, and two systems for, glycine betaine transport by Staphylococcus aureus

Cited by 30 publications

References 11 publications

Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals

Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals

Isolation, characterization, and expression of the Corynebacterium glutamicum betP gene, encoding the transport system for the compatible solute glycine betaine

A Postgenomic Appraisal of Osmotolerance in Listeria monocytogenes

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