Department of Food Science and Technology,
University of Nebraska, Lincoln, Nebraska 68583-0919
 |
TEXT |
Listeria monocytogenes is
a ubiquitous, psychrotrophic food-borne pathogen capable of causing
highly invasive infections in humans resulting in septicemia,
meningitis, and spontaneous abortions (29). This organism is
problematic for the food production industry due to its ubiquitous
distribution in nature and its ability to grow at temperatures ranging
from 4 to 45°C (14, 32, 40) and in salt concentrations
ranging from 10 to 20% (12, 14, 24).
Two different types of adaptive responses to low temperature have been
described thus far for L. monocytogenes. One of the responses is accomplished by adjusting membrane fluidity through alteration of the membrane fatty acid composition (3). A
second response is manifest by the accumulation of compatible solutes such as glycine betaine, carnitine, and proline by uptake from the
environment (7, 21). L. monocytogenes accumulates
betaine and carnitine via biochemically distinct transporters (7,
17, 21, 26, 34, 35, 36). Genes encoding two different betaine transporters, GbuA (22) and BetL (33), have
recently been cloned and demonstrated to encode homologues of
ATP-dependent and ion-driven transporters, respectively. The structure
of the carnitine transporter(s) is unknown, but biochemical studies
demonstrate the existence of an ATP-dependent system (36).
Accumulation of compatible solutes is a common response to osmotic
upshift in many species (7, 15, 18, 21, 23, 25), and these
solutes presumably alleviate the consequences of osmotic stress by
maintaining favorable osmotic pressure without altering the structure
of intracellular proteins and other cellular machinery (4,
42). It is unclear if the solutes play the same roles in
adaptation to low temperature or if the same machinery governs their
accumulation under the physiologically distinct osmotic and temperature
stress conditions.
One regulatory factor that could coordinate both osmotic and
low-temperature stress responses in L. monocytogenes is the
general stress sigma factor 
B, whose activity is
stimulated in response to osmotic upshift and temperature downshift
(5). In the related species Bacillus subtilis,
B is known to control transcription of a large general
stress regulon, whose products include different classes of proteins
that alleviate the physiological consequences of environmental and
nutritional stress conditions (19). The activity of
B is stimulated by a wide variety of physical signals
and is coupled to these signals by a complex cascade of eight different
Rsb proteins that modulate the binding of B to its
primary regulator through a series of protein-protein interactions and
phosphate transfers (1, 2, 6, 8, 9, 13, 20, 37, 38, 41, 43).
The homology that is observed in the amino acid sequences of the
B and Rsb protein homologues in L. monocytogenes and B. subtilis suggests that
B is regulated similarly in each organism. However,
activation of B in L. monocytogenes is
acutely responsive to temperature and osmotic stress, whereas its
activity in B. subtilis is only modestly induced in the case
of osmolarity and not detectable in the case of rapid cold shock
(5, 9). This indicates that the activity and function of the
B regulon may be fine-tuned to the physiology of the
host organism. In the present study, we sought to characterize the
unique role that B plays in adaptation of L. monocytogenes to low temperatures.
Low-temperature activation of B in L. monocytogenes.
Since the growth pattern of L. monocytogenes after a temperature downshift is complex, we first
compared growth and the appearance of B activity after
the cells were subjected to a temperature downshift from 37 to 8°C
(Fig. 1). When logarithmically growing
cells were temperature downshifted, the cells rapidly ceased growing
and did not assume a new growth rate until about 6 h after the
shift. Primer extension analysis of transcripts originating from the B-dependent rsbV promoter (5)
showed that the appearance of detectable transcript corresponded with
the new growth rate (Fig. 1). RNA samples extracted from cells prior to
the temperature downshift were devoid of detectable transcript. The
transcript was also absent from samples after 15, 30, and 60 min of
incubation (data not shown) but began to accumulate after 2 h with
a substantial increase at the 6-h time point, the time at which the
cells assumed a new growth rate.
View larger version (38K):
[in this window]
[in a new window]
|
FIG. 1.
Primer extension analysis of the pattern of
B induction in L. monocytogenes after
temperature downshift. Strain 10403S was grown in brain heart infusion
to mid-logarithmic phase at 37°C followed by temperature downshift to
8°C. Growth was determined by measuring OD600, and values
obtained after cold shock are shown on the graph. Primer extension
analysis was used to measure the activity of B at the
rsbV promoter. At times indicated by arrows on the graph,
RNA was extracted from an aliquot of cells and 50 µg was used as a
template for extension of the labeled VPROM2 primer (5). The
numbers over the lanes in the autoradiograph correspond to the times
indicated in the graph. A sequencing ladder generated with the same
primer is shown to the left of the extension products.
|
|
Because B activity usually appears within 20 min of a
stress signal in either L. monocytogenes or B. subtilis (5, 9), the delay in activation after cold
shock was unanticipated. The cold-induced lag could be caused by the
absence of B activity; however, data presented below are
not consistent with this explanation. Alternatively, the function of
one or more proteins necessary to elicit B activity may
be impaired by cold shock. In support of the latter hypothesis,
ribosome integrity or function is required for the relay of
environmental stress to B in B. subtilis
(30, 31). If B activity is linked to ribosome
function in L. monocytogenes, then the delay in activity
could be a consequence of the time necessary to reassemble, repair,
and/or resynthesize cold-damaged ribosomes. Preliminary
pulse-labeling experiments with L. monocytogenes are consistent with this explanation since the rate of translation falls 10-fold during the lag period following a cold shock and does not
approach preshock levels until the cells assume a new growth rate, much
like the appearance of B activity (L. A. Becker and
A. K. Benson, unpublished data).
Role of B in low-temperature adaptation.
To
determine whether B activity is necessary for growth at
low temperatures, growth rates of log-phase cultures of the wild-type strain 10403S and the isogenic sigB::Km null
mutant LMA2B (5) were measured in a defined medium (DM)
(5, 7, 28) before and after a temperature downshift. Both
strains displayed comparable lag periods after the downshift, and as
shown in Table 1, their growth rates were
nearly identical after growth was reinitiated at the lower temperature.
Since the lag periods were nearly identical in both strains, it is
unlikely that delayed activation of B in the wild-type
strain (Fig. 1) is the cause of the lag. Thus, even though the
appearance of B activity coincides with the pattern of
growth after temperature downshift, its function is not essential for
adaptation of log-phase cells.
Since we had previously shown that B function was
required for osmotically induced accumulation of betaine, we next
tested whether B activity contributes to uptake and
utilization of betaine and carnitine as cryoprotectants at low
temperatures. When 1 mM betaine or carnitine was added to the cultures
of 10403S at the time of temperature downshift, the growth rate
increased from 0.09 to 0.18 and 0.17 h
1, respectively
(Table 1). Addition of betaine or carnitine to the
sigB::Km strain, LMA2B (Table 1), did not have a
statistically significant effect on growth, indicating that
B activity contributes to utilization of betaine and
carnitine as cryoprotectants.
To test whether betaine and carnitine uptake is defective in the
sigB mutant, accumulation of radiolabeled betaine and
carnitine was measured before and after a temperature downshift.
Cultures were grown at 37°C in DM to mid-logarithmic phase (optical
density at 600 nm [OD600], ~0.4), and then aliquots
were removed and immediately shifted to 25 and 8°C for 5 min followed
by addition of 1 mM [14C]betaine (65 µCi/mmol) or 1 mM
[3H]carnitine (118 µCi/mmol). As shown in Fig.
2, betaine accumulated in the wild-type
cells to comparable levels at both temperatures whereas carnitine
accumulation was higher at 25°C. In contrast, accumulation of both
betaine and carnitine was impaired in LMA2B at both temperatures. We
conclude that, in log-phase cells, the principal contribution of
B to low-temperature growth is to modulate the
accumulation of compatible solutes.
View larger version (13K):
[in this window]
[in a new window]
|
FIG. 2.
Cryoprotectant accumulation in 10403S and LMA2B at room
temperature and immediately following temperature downshift. Cells were
grown in DM at 37°C to mid-logarithmic phase (OD600,
~0.4), followed by immediate temperature downshift to 8°C. Prior to
temperature shift and after acclimating for 5 min at 8°C, cell
suspensions were collected and adjusted to approximately 0.12 mg of
protein/ml. Uptake assays were performed at either 25°C (A) or 8°C
(B) and started by addition of [14C]betaine or
[3H]carnitine to each sample. Aliquots were removed over
the time of the assay, harvested by centrifugation through oil, and
counted by scintillation counting. Symbols:  , 10403S plus
[14C]betaine;  , 10403S plus
[3H]carnitine;  , LMA2B plus
[14C]betaine;  , LMA2B plus
[3H]carnitine.
|
|
Role of B in low-temperature adaptation of
stationary-phase cells.
Because B activity is
stimulated by onset of stationary phase, we next tested whether it
might play unique roles in adaptation of stationary-phase cells to
low-temperature environments. Overnight cultures of 10403S and LMA2B
were grown at 37°C in DM and subsequently inoculated into fresh DM
and incubated at 8°C. The resulting growth curves showed that the
absence of B impaired adaptation of stationary-phase
cells to growth at the lower temperature (Fig.
3). The parental strain 10403S exhibited a lag phase lasting approximately 4 days, while that of LMA2B was
nearly twice as long, lasting approximately 8 days. These results imply
that, in contrast to log-phase cells, B plays an
important role in adaptation of stationary-phase cells to
low-temperature growth.
View larger version (13K):
[in this window]
[in a new window]
|
FIG. 3.
Growth of 10403S and LMA2B at 8°C in the presence of
cryoprotectants. Overnight stationary-phase cultures of 10403S and
LMA2B growing in DM at 37°C were used to inoculate fresh DM
supplemented with 1 mM betaine (A) or 1 mM carnitine (B) and incubated
at 8°C. Symbols: , 10403S with no cryoprotectant; , LMA2B with
no cryoprotectant; , 10403S with 1 mM betaine; , LMA2B with 1 mM
betaine;  , 10403S with 1 mM carnitine;  , LMA2B with 1 mM
carnitine.
|
|
Given the different phenotypes of log- and stationary-phase cells of
the sigB::Km strain, we suggest that L. monocytogenes has independent pathways for adaptation to growth at
low temperature. One pathway is B independent and can be
entered into by log-phase cells, while the second pathway has a
B-dependent component and is the pathway of choice in
stationary-phase cells. Alternatively, a single pathway for adaptation
may exist, with genes that participate in the pathway having
B-independent modes of expression during log phase and
B-dependent modes of expression that operate during
stationary phase. Growth phase-dependent roles of B have
also been reported for B. subtilis (16), and
together, these data suggest that B may constitute a
general device for controlling growth phase-dependent pathways of
stress response.
When 1 mM betaine was added at the time of inoculation, the lag phase
of both 10403S and LMA2B decreased (Fig. 3A); however, the decrease was
more pronounced in the wild-type strain. Once LMA2B resumed growth in
the presence of betaine, its rate was indistinguishable from that of
the wild type. Addition of carnitine decreased the lag phase of both
10403S and LMA2B to nearly identical times (Fig. 3B). Thus, although
B is necessary for efficient utilization of carnitine
and betaine in log-phase cells, it is apparently necessary only for
utilization of betaine in stationary-phase cells.
To test whether B is necessary for efficient uptake of
betaine and carnitine in stationary-phase cells, accumulation was
measured in cells that were grown from inoculation at 8°C. Overnight
cultures growing at 37°C in DM were used to inoculate fresh DM
followed by incubation at 8°C. Upon reaching mid-logarithmic growth,
aliquots were removed and uptake of radiolabeled betaine or carnitine
was measured. Figure 4 shows that there
was considerably less accumulation of both betaine and carnitine in
LMA2B compared to the wild-type strain, 10403S. Surprisingly, however,
carnitine accumulation was defective in the sigB mutant
growing at 8°C, even though the mutant's ability to utilize
carnitine as a cryoprotectant (Fig. 3B) did not reflect its diminished
ability to accumulate it. This supports the conclusion that residual
carnitine transport in stationary-phase cells in the absence of
B is sufficient to provide cryoprotection and implies
that carnitine is a more efficient cryoprotectant than betaine.
View larger version (15K):
[in this window]
[in a new window]
|
FIG. 4.
Cryoprotectant accumulation in 10403S and LMA2B growing
at 8°C. Overnight stationary-phase cultures of 10403S and LMA2B
growing in DM at 37°C were used to inoculate fresh DM followed by
incubation at 8°C. Cells in mid-logarithmic growth
(OD600, ~0.4) were collected, and cell suspensions were
adjusted to approximately 0.12 mg of protein/ml. Uptake assays were
performed at 8°C and started by addition of
[14C]betaine or [3H]carnitine to each
sample. Aliquots were removed over the time of the assay, harvested by
centrifugation through oil, and counted by scintillation counting.
Symbols: , 10403S plus [14C]betaine; , 10403S plus
[3H]carnitine; , LMA2B plus
[14C]betaine; , LMA2B plus
[3H]carnitine.
|
|
The relative efficiencies of carnitine and betaine as osmoprotectants
and cryoprotectants have been examined with Escherichia coli
and L. monocytogenes. Betaine is a better osmoprotectant than carnitine in E. coli, presumably because the longer
carbon chain length of carnitine decreases its osmoprotective function (27). For wild-type L. monocytogenes, betaine has
been reported to be more effective than carnitine in providing
tolerance to low temperature (34), despite the fact that
more carnitine accumulates at low temperatures than does betaine
(21). It may be that a low threshold of carnitine
accumulation is necessary to promote low-temperature growth of
stationary-phase L. monocytogenes cells and that residual
uptake in the sigB::Km strain is enough to sustain wild-type levels of growth. Betaine and carnitine may also have different roles in cryoprotection. In eukaryotic cells, carnitine stimulates beta-oxidation of lipids by serving as a carrier across the
mitochondria (4). It is conceivable that carnitine could also function as a carrier in the process of fatty acid alteration that
occurs during low-temperature adaptation of L. monocytogenes. If it were to play a role as a cofactor, then it
might be needed only at modest concentrations.
Since two different betaine transport systems have been described
biochemically and genetically (17, 22), it is possible that
B could exert its effects by influencing the activity of
one or both systems. To address this question, we used a physiological approach to determine the sensitivity of the residual betaine transport
to metabolic inhibitors in the absence of B. The BetL
system of betaine transport is sodium dependent and sensitive to the
effects of monensin, a sodium ionophore (17), whereas the
GbuA transport system is ATP dependent (22) and therefore
insensitive to the immediate effects of monensin. When 0.02 mM monensin
was added to cold-grown cell suspensions (Table 2), the rate of betaine transport by the
wild-type strain, 10403S, was reduced by only 20%, indicating that,
under these growth conditions, the majority of the transport was
mediated by the GbuA-dependent system (assuming that GbuA is the only
monensin-resistant betaine transport system in L. monocytogenes). Addition of monensin to the sigB
mutant, however, inhibited betaine transport by more than 90%. This
result suggests that residual betaine transport in the sigB
mutant is BetL dependent and implies that B influences
betaine transport primarily through the GbuA transporter. Although the
promoter regions of betL and gbuA have not been
identified experimentally, a sequence similar to
B-dependent promoters was identified upstream of the
betL gene (33), while no B-like
element could be found upstream of gbuA (22). We
have identified a substrate-inducible, B-independent
promoter upstream of betL but have not been able to observe
a transcript that originates from the putative
B-dependent promoter under any condition tested (M. S. Cetin and A. K. Benson, unpublished). We are currently examining
transcription from the gbuA and betL promoters to
precisely determine how B influences betaine transport.
The role of B in carnitine accumulation is less clear
than that of betaine, since no carnitine transport systems have been cloned from L. monocytogenes. Although Verheul et al.
(36) reported the presence of an ATP-dependent carnitine
transport system in L. monocytogenes strain Scott A,
carnitine transport in our experiments was inhibited by monensin to the
same extent in both wild-type and mutant cells, leading us to conclude
that a sodium-dependent system may be primarily responsible for
transport of this cryoprotectant.
This research was supported, in part, by funds from USDA HATCH
project no. NEB-16-077 and the Midwest Alliance for Food Manufacturing. S.N.E. is supported by USDA National Needs Fellowship no.
96-38420-3050.
| 1.
|
Akbar, S.,
C. M. Kang,
T. A. Gaidenko, and C. W. Price.
1997.
Modulator protein RsbR regulates environmental signaling in the general stress pathway of Bacillus subtilis.
Mol. Microbiol.
24:567-578[CrossRef][Medline].
|
| 2.
|
Alper, S.,
L. Duncan, and R. Losick.
1994.
An adenosine nucleotide switch controlling the activity of a cell type-specific transcription factor in Bacillus subtilis.
Cell
77:195-205[CrossRef][Medline].
|
| 3.
|
Annous, B. A.,
L. A. Becker,
D. O. Bayles,
D. P. Labeda, and B. J. Wilkinson.
1997.
Critical role of anteiso-C15:0 fatty acid in the growth of Listeria monocytogenes at low temperature.
Appl. Environ. Microbiol.
63:3887-3894[Abstract].
|
| 4.
|
Anthoni, U.,
C. Christophersen,
L. Hougaard, and P. H. Nielsen.
1991.
Quaternary ammonium compounds in the biosphere an example of a versatile adaptive strategy.
Comp. Biochem. Physiol.
99B:1-18.
|
| 5.
|
Becker, L. A.,
M. S. Cetin,
R. W. Hutkins, and A. K. Benson.
1998.
Identification of the gene encoding the alternative sigma factor B from Listeria monocytogenes and its role in osmotolerance.
J. Bacteriol.
180:4547-4554[Abstract/Free Full Text].
|
| 6.
|
Benson, A. K., and W. G. Haldenwang.
1993.
Bacillus subtilis B is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase.
Proc. Natl. Acad. Sci. USA
90:2330-2334[Abstract/Free Full Text].
|
| 7.
|
Beumer, R. R.,
M. C. Te Giffel,
L. J. Cox,
F. M. Rombouts, and T. Abee.
1994.
Effect of exogenous proline, betaine, and carnitine on growth of Listeria monocytogenes in a minimal medium.
Appl. Environ. Microbiol.
60:1359-1363[Abstract/Free Full Text].
|
| 8.
|
Boylan, S. A.,
A. R. Redfield, and C. W. Price.
1993.
Transcription factor B of Bacillus subtilis controls a large stationary-phase regulon.
J. Bacteriol.
175:3957-3963[Abstract/Free Full Text].
|
| 9.
|
Boylan, S. A.,
A. R. Redfield,
M. S. Brody, and C. W. Price.
1993.
Stress-induced activation of the B transcription factor of Bacillus subtilis.
J. Bacteriol.
175:7931-7937[Abstract/Free Full Text].
|
| 10.
|
Chomczynski, P., and N. Sacchi.
1987.
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
Anal. Biochem.
162:156-159[Medline].
|
| 11.
|
Christensen, D. P.,
A. K. Benson, and R. W. Hutkins.
1998.
Cloning and expression of the Listeria monocytogenes Scott A ptsH and ptsI genes, coding for Hpr and enzyme I, respectively, of the phosphotransferase system.
Appl. Environ. Microbiol.
64:3147-3152[Abstract/Free Full Text].
|
| 12.
|
Cole, M. B.,
M. V. Jones, and C. Holyoak.
1990.
The effect of pH, salt concentration and temperature on the survival and growth of Listeria monocytogenes.
J. Appl. Bacteriol.
69:63-72[Medline].
|
| 13.
|
Dufour, A., and W. G. Haldenwang.
1994.
Interactions between a Bacillus subtilis anti-sigma factor (RsbW) and its antagonist (RsbV).
J. Bacteriol.
176:1813-1820[Abstract/Free Full Text].
|
| 14.
|
Farber, J. M., and P. I. Peterkin.
1991.
Listeria monocytogenes, a food-borne pathogen.
Microbiol. Rev.
55:476-511[Abstract/Free Full Text].
|
| 15.
|
Farwick, M.,
R. M. Siewe, and R. Krämer.
1995.
Glycine betaine uptake after hyperosmotic shift in Corynebacterium glutamicum.
J. Bacteriol.
177:4690-4695[Abstract/Free Full Text].
|
| 16.
|
Gaidenko, T. A., and C. W. Price.
1998.
General stress transcription factor B and sporulation sigma factor H contribute to survival of Bacillus subtilis under extreme growth conditions.
J. Bacteriol.
180:3730-3733[Abstract/Free Full Text].
|
| 17.
|
Gerhardt, P. N. M.,
L. T. Smith, and G. M. Smith.
1996.
Sodium-driven, osmotically activated glycine betaine transport in Listeria monocytogenes membrane vesicles.
J. Bacteriol.
178:6105-6109[Abstract/Free Full Text].
|
| 18.
|
Graham, J. E., and B. J. Wilkinson.
1992.
Staphylococcus aureus osmoregulation: roles for choline, glycine betaine, proline, and taurine.
J. Bacteriol.
174:2711-2716[Abstract/Free Full Text].
|
| 19.
|
Hecker, M., and U. Völker.
1998.
Non-specific, general and multiple stress resistance of growth-restricted Bacillus subtilis cells by the expression of the B regulon.
Mol. Microbiol.
29:1129-1136[CrossRef][Medline].
|
| 20.
|
Kang, C. M.,
M. S. Brody,
S. Akbar,
X. Yang, and C. W. Price.
1996.
Homologous pairs of regulatory proteins control activity of Bacillus subtilis transcription factor B in response to environmental stress.
J. Bacteriol.
178:3846-3853[Abstract/Free Full Text].
|
| 21.
|
Ko, R.,
L. T. Smith, and G. M. Smith.
1994.
Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes.
J. Bacteriol.
176:426-431[Abstract/Free Full Text].
|
| 22.
|
Ko, R., and L. T. Smith.
1999.
Identification of an ATP-driven, osmoregulated glycine betaine transport system in Listeria monocytogenes.
Appl. Environ. Microbiol.
65:4040-4048[Abstract/Free Full Text].
|
| 23.
|
Landfald, B., and A. R. Strom.
1986.
Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli.
J. Bacteriol.
165:849-855[Abstract/Free Full Text].
|
| 24.
|
Miller, A. J.
1992.
Combined water activity and solute effects on growth and survival of Listeria monocytogenes Scott A.
J. Food Prot.
55:414-418.
|
| 25.
|
Molenaar, D.,
A. Hagting,
H. Alkema,
A. J. M. Driessen, and W. N. Konings.
1993.
Characterististics and osmoregulatory roles of uptake systems for proline and glycine betaine in Lactococcus lactis.
J. Bacteriol.
175:5438-5444[Abstract/Free Full Text].
|
| 26.
|
Patchett, R. A.,
A. F. Kelly, and R. G. Kroll.
1994.
Transport of glycine-betaine by Listeria monocytogenes.
Arch. Microbiol.
162:205-210[Medline].
|
| 27.
|
Peddie, B. A.,
M. Lever,
C. M. Hayman,
K. Randall, and S. T. Chambers.
1994.
Relationship between osmoprotection and the structure and intracellular accumulation of betaines by Escherichia coli.
FEMS Microbiol. Lett.
120:125-132[CrossRef][Medline].
|
| 28.
|
Pine, L.,
G. B. Malcom,
J. B. Brooks, and M. I. Daneshvar.
1989.
Physiological studies on the growth and utilization of sugars by Listeria species.
Can. J. Microbiol.
35:245-254[Medline].
|
| 29.
|
Schuchat, A.,
B. Swaminathan, and C. V. Broome.
1991.
Epidemiology of human listeriosis.
Clin. Microbiol. Rev.
4:169-183[Abstract/Free Full Text].
|
| 30.
|
Scott, J. M., and W. G. Haldenwang.
1999.
Obg, an essential GTP binding protein of Bacillus subtilis, is necessary for stress activation of transcription factor B.
J. Bacteriol.
181:4653-4660[Abstract/Free Full Text].
|
| 31.
|
Scott, J. M.,
J. Ju,
T. Mitchell, and W. G. Haldenwang.
2000.
The Bacillus subtilis GTP binding protein Obg and regulators of the B stress response transcription factor cofractionate with the ribosomes.
J. Bacteriol.
182:2771-2777[Abstract/Free Full Text].
|
| 32.
|
Seeliger, H. P. R., and D. Jones.
1986.
Listeria, p. 1235-1245.
In
P. H. A. Sneath, N. S. Mair, M. E. Sharpe, and J. G. Holt (ed.), Bergey's manual of systematic bacteriology, vol. 2. Williams & Wilkins, Baltimore, Md.
|
| 33.
|
Sleator, R. D.,
C. G. M. Gahan,
T. Abee, and C. Hill.
1999.
Identification and disruption of BetL, a secondary glycine betaine transport system linked to the salt tolerance of Listeria monocytogenes LO28.
Appl. Environ. Microbiol.
65:2078-2083[Abstract/Free Full Text].
|
| 34.
|
Smith, L. T.
1996.
Role of osmolytes in adaptation of osmotically stressed and chill-stressed Listeria monocytogenes grown in liquid media and on processed meat surfaces.
Appl. Environ. Microbiol.
62:3088-3093[Abstract].
|
| 35.
|
Verheul, A.,
E. Glaasker,
B. Poolman, and T. Abee.
1997.
Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals.
J. Bacteriol.
179:6979-6985[Abstract/Free Full Text].
|
| 36.
|
Verheul, A.,
F. M. Rombouts,
R. R. Beumer, and T. Abee.
1995.
An ATP-dependent L-carnitine transporter in Listeria monocytogenes Scott A is involved in osmoprotection.
J. Bacteriol.
177:3205-3212[Abstract/Free Full Text].
|
| 37.
|
Vijay, K.,
M. S. Brody,
E. Fredlund, and C. W. Price.
2000.
A PP2C phosphatase containing a PAS domain is required to convey signals of energy stress to the B transcription factor of Bacillus subtilis.
Mol. Microbiol.
35:180-188[CrossRef][Medline].
|
| 38.
|
Voelker, U.,
A. Voelker,
B. Maul,
M. Hecker,
A. Dufour, and W. G. Haldenwang.
1995.
Separate mechanisms activate B of Bacillus subtilis in response to environmental and metabolic stress.
J. Bacteriol.
177:3771-3780[Abstract/Free Full Text].
|
| 39.
|
Waite, B. L.,
G. R. Siragusa, and R. W. Hutkins.
1998.
Bacteriocin inhibition of two glucose transport systems in Listeria monocytogenes.
J. Appl. Microbiol.
84:715-721[CrossRef][Medline].
|
| 40.
|
Walker, S. J.,
P. Archer, and J. G. Banks.
1990.
Growth of Listeria monocytogenes at refrigeration temperatures.
J. Appl. Bacteriol.
68:157-162[Medline].
|
| 41.
|
Wise, A. A., and C. W. Price.
1995.
Four additional genes in the sigB operon of Bacillus subtilis that control activity of the general stress factor B in response to environmental signals.
J. Bacteriol.
177:123-133[Abstract/Free Full Text].
|
| 42.
|
Yancey, P. H.,
M. E. Clark,
S. C. Hand,
R. D. Bowlus, and G. N. Somero.
1982.
Living with water stress: evolution of osmolyte systems.
Science
217:1214-1222[Abstract/Free Full Text].
|
| 43.
|
Yang, X.,
C. M. Kang,
M. S. Brody, and C. W. Price.
1996.
Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor.
Genes Dev.
10:2265-2275[Abstract/Free Full Text].
|
![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
B in Adaptation of
Listeria monocytogenes to Growth at Low
Temperature
Top
Abstract
Text
Paper no. 13140, Journal Series Nebraska Agricultural Experimental
Station, Lincoln, NE 69583-0919.
