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Applied and Environmental Microbiology, December 1999, p. 5328-5333, Vol. 65, No. 12
Institut National de la Recherche
Agronomique, Unité de Recherche en Bioadhesion et Hygiène
des Materiaux, Massy,1 and SKW
Biosystems, Cultures & Enzymes Department, La Ferté sous
Jouarre,2 France, and University
College, Cork, Ireland3
Received 9 November 1998/Accepted 15 September 1999
We determined the variations in the surface physicochemical
properties of Listeria monocytogenes Scott A cells that
occurred under various environmental conditions. The surface charges,
the hydrophobicities, and the electron donor and acceptor
characteristics of L. monocytogenes Scott A cells were
compared after the organism was grown in different growth media and at
different temperatures; to do this, we used microelectrophoresis and
the microbial adhesion to solvents method. Supplementing the growth
media with glucose or lactic acid affected the electrical, hydrophobic,
and electron donor and acceptor properties of the cells, whereas the
growth temperature (37, 20, 15, or 8°C) primarily affected the
electrical and electron donor and acceptor properties. The nonlinear
effects of the growth temperature on the physicochemical properties of the cells were similar for cells cultivated in two different growth media, but bacteria cultivated in Trypticase soy broth supplemented with 6 g of yeast extract per liter (TSYE) were slightly more hydrophobic than cells cultivated in brain heart infusion medium (P < 0.05). Adhesion experiments conducted with
L. monocytogenes Scott A cells cultivated in TSYE at 37, 20, 15, and 8°C and then suspended in a sodium chloride solution
(1.5 × 10 Listeria monocytogenes is
a gram-positive human pathogen that is responsible for serious
infections in immunocompromised individuals and pregnant women
(17). L. monocytogenes has been implicated in
several food-borne disease outbreaks. This organism is found not only
in raw food but also on working surfaces in food-processing plants
(40, 41). Microorganisms attached to a surface are an
important potential source of contamination for any food material coming into contact with that surface (27). Bacterial
attachment to an inert surface results from complex physicochemical
interactions among the cell, the surface, and the liquid phase
(24), which are caused by the cell surface charge
(15), the hydrophobicity (45), and electron
acceptor and donor properties (47).
Many workers have described the effects of various environmental
parameters on L. monocytogenes growth (1, 7, 13), survival (31, 32, 34), pathogenicity (14, 44),
and adhesion (2, 24). The most frequently studied parameters
are growth temperature (12, 39), acidification of the growth
media with organic acids (20, 43), and changes in the water
activity of the growth medium caused by adding NaCl (29,
33). It has also been shown that results may be depend on the
growth medium (16, 21, 25). For L. monocytogenes
growth, the following two media have been used most frequently
previously: brain heart infusion (BHI) broth (4, 30) and
Trypticase soy broth supplemented with 6 g of yeast extract per
liter (TSYE) (5, 22, 26).
Limited data concerning the effects of environmental and cultivation
parameters on the physicochemical properties of L. monocytogenes have been published previously. Hence, the aim of
this study was to determine the surface electrical properties,
hydrophobicities, and electron donor and acceptor properties of
L. monocytogenes Scott A cells under different growth conditions.
Bacterial strains, growth conditions, and preparation of
microbial suspension.
L. monocytogenes Scott A (a human
isolate obtained from the 1983 Massachusetts milk outbreak
[18]) was provided by Bongrain Research and
Development Centre (SOREDAB, La Boissière Ecole, France) and was
stored at
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Listeria monocytogenes Scott A: Cell
Surface Charge, Hydrophobicity, and Electron Donor and Acceptor
Characteristics under Different Environmental Growth
Conditions
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
1 or 1.5 × 103 M NaCl)
confirmed that the cell surface charge and the electron donor and
acceptor properties of the cells had an influence on their attachment
to stainless steel.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
80°C.
1 or 1.5 × 103 M NaCl).
MATS.
Microbial adhesion to solvents (MATS) is based on
comparing microbial cell affinity to a polar solvent and microbial cell affinity to a nonpolar solvent (8). The polar solvent can be an electron acceptor or an electron donor, but both solvents must have
similar van der Waals surface tension components. The following pairs
of solvents, as described by Bellon-Fontaine et al. (8), were used: chloroform, an electron acceptor solvent, and hexadecane, a
nonpolar solvent; and ethyl acetate, a strong electron donor solvent,
and decane, a nonpolar solvent. Due to the surface tension properties
of these solvents, differences between the results obtained with
chloroform and hexadecane and the results obtained with ethyl acetate
and decane indicated that there were electron donor-electron acceptor
interactions at the bacterial cell surface and revealed hydrophobic and
hydrophilic properties. A microbial suspension containing approximately
108 CFU in 2.4 ml of 1.5 × 101 M NaCl
was vortexed for 60 s with 0.4 ml of a solvent. This high concentration of electrolyte was used to avoid charge interference by a
masking cell charge, because some solvent droplets, especially hexadecane, become negatively charged in aqueous suspensions
(19). The mixture was allowed to stand for 15 min to ensure
that the two phases were completely separated before a sample (1 ml)
was carefully removed from the aqueous phase and the optical density at
400 nm was determined. The percentage of cells present in each solvent
was subsequently calculated by using the equation: % Affinity = 100 × [1 (A/A0)], where
A0 is the optical density at 400 nm of the
bacterial suspension before mixing and A is the absorbance
after mixing. Each experiment was performed in triplicate by using
three independently prepared cultures.
Electrophoretic mobility.
To measure electrophoretic
mobility, bacteria were suspended in 1.5 × 103 M
sodium chloride at a concentration of 107 CFU · ml1. The pH of the suspension was adjusted to pH 2 to 7 by adding nitric acid (HNO3) or potassium hydroxide (KOH).
Electrophoretic mobility was measured by using a 50-V electric field
and a Laser Zetameter (Zêtaphoremètre II;
Société d'Étude Physico-Chimiques, Limours, France).
The results were based on an automated video analysis of about 200 particles for each measurement. Each experiment was performed in
duplicate by using two independently prepared cultures. The typical
standard deviation for the electrophoretic mobility mean was 0.25 µm/V/cm/s.
Microbial adhesion to AISI 304 stainless steel. (i) Solid surface and cleaning treatment. The solid support selected for this study was AISI 304 stainless steel (Goodfellow, Cambridge Science Park, United Kingdom). Before physicochemical characterization and adhesion assays were begun, the steel was cut into rectangular chips (3 by 1 cm) and cleaned by soaking for 10 min at 50°C in a 2% (vol/vol) solution of the commercial surfactant RBS 35 (Société des Traitements Chimiques de Surface, Lambersart, France), rinsing for 10 min in Milli-Q water (Millipore, Saint-Quentin en Yvelines, France) at 50°C, and rinsing five times in 500 ml of Milli-Q water at room temperature.
(ii) Determination of the physicochemical properties of the solid
surface.
The Lifshitz-van der Waals (
LW), electron
donor (), and electron acceptor (+)
surface tension components of stainless steel (S) were
determined by measuring contact angles by using the approach proposed
by van Oss et al. (46). In this approach, in which spreading
pressure is ignored, the contact angles (
), measured with three pure
liquids (L), can be expressed as:
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(iii) Adhesion experiments.
Adhesion assays were performed
by using microbial cells cultured at 37, 20, 15, or 8°C in TSYE and
resuspended in 1.5 × 101 or 1.5 × 103 M sodium chloride as described below. Thirty
milliliters of a bacterial suspension containing approximately
108 CFU · ml1 was incubated in a petri
dish (diameter, 10 cm) containing 3-cm2 stainless steel
chips for 3 h at the temperature at which the bacteria were grown
(37, 20, 15, or 8°C). The stainless steel chips were then rinsed to
remove the nonadhering bacteria by pouring 30 ml of Milli-Q water onto
the chips three times. The stainless steel chips were immersed in a
test tube containing 10 ml of sterile 1.5 × 101 or
1.5 × 103 M NaCl. Bacterial cells were detached
from the inert support by using a sonication bath (Ultrasonik) for 2 min at 40 kHz and 35°C. CFUs were counted by using the serial
dilution technique and the bacterial suspension obtained after
sonication. Counts were determined on TSYE agar (Biomérieux), and
the preparations were incubated for 24 h at 37°C. Each
experiment was performed in triplicate by using two independently grown
cultures. We assessed the viability of the bacteria in the two
suspending liquids and at the four temperatures analyzed by counting
suspended cells on TSYE agar at the beginning and end of the adhesion period.
Statistical analysis. A principal-component analysis was performed by using STATITCF software (Institut Technique des Céréales et des Fourrages, Paris, France), and a two-way analysis of variance was performed with Statgraphics 6.0 (Manugistics, Rockville, Md.).
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Influence of growth conditions (medium and temperature) on L. monocytogenes Scott A surface physicochemical properties. (i)
Influence of growth medium on cell surface physicochemical
properties.
The MATS results obtained for L. monocytogenes Scott A grown at 37°C in BHI, TSYE, TSYE
supplemented with glucose, and TSYE supplemented with lactic acid are
shown in Table 1. Regardless of the
medium used, the affinity of L. monocytogenes Scott A was always higher with chloroform (an electron acceptor solvent) than with
hexadecane (a nonpolar solvent). The differences in bacterial affinity
between these two solvents were due to Lewis acid-base interactions
(i.e., electron donor-electron acceptor interactions resulting from the
electron donor nature of the bacteria). The electron donor nature was
maximized for cells cultivated in BHI medium or TSYE. Likewise,
bacterial affinity was lower with ethyl acetate (a strongly
electron-donating solvent) than with decane, indicating that the
electron-accepting nature of L. monocytogenes Scott A grown
in either medium was weak. Affinity to ethyl acetate was maximized with
cells cultivated in the glucose-supplemented medium; this culture was
also the culture with the lowest pH in the stationary phase (pH 4.1 and
4.7 for culture media supplemented with glucose and lactic acid,
respectively; pH 5.1 for cells grown in TSYE).
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(ii) Influence of growth temperature on cell surface
physicochemical properties.
Table 1 shows the affinities with the
four solvents used in the MATS method of the bacteria grown in TSYE or
BHI medium at 37, 20, 15, and 8°C. Cells cultivated in TSYE exhibited
slightly greater affinity with nonpolar solvents than cells cultivated in BHI medium exhibited (P < 0.05), and the affinity
with ethyl acetate was greatest at 37°C and least at 15°C
(P < 0.05). Moreover, the growth temperature had a
significant effect (P < 0.05) on the electrophoretic
mobility of the bacteria, as shown in Fig. 2. Our results indicated that the
nonlinear effects of the growth temperature on the electrophoretic
mobility of microbial cells were the same for both growth media. Except
for the most acidic pH (pH 2.0), electrophoretic mobility was greatest
for cells grown at 15 or 20°C and lowest for cells cultivated at
8°C. The electrophoretic mobility of the bacteria was between 0.5
and 2 µm/s/V/cm at pH 2.0. The isoelectric point of microbial cells
could not be determined at any of the growth temperatures used in this
study. Data were analyzed by using the data compression step of
principal-component analysis, which removes the redundancy in an
original data set so that only the first few principal-component scores
are needed to describe most of the information in the original
data set (11). The results of a principal-component analysis
of the combined physicochemical properties of L. monocytogenes Scott A grown in TSYE or BHI medium at all
temperatures are shown in Fig. 3. The first principal-component score, which accounts for 43% of the total
variation in the original data set, is positively correlated with a
high negative cell wall charge. This principal-component score
discriminates among the samples by relating to the growth temperature.
The second principal-component score represents 29% of the total
variation in the original data set, and it is positively correlated
with cell affinity for nonpolar solvents (hexadecane and decane) and
negatively correlated with cell affinity for ethyl acetate. This
principal-component score mainly distinguishes between cells grown in
BHI and cells grown in TSYE.
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) and BHI medium
(
). The first principal component (principal component 1) was
positively correlated with a high negative charge of bacterial cells.
The second principal component (principal component 2) was positively
correlated with bacterial cell affinity for nonpolar solvents and
negatively correlated with cell affinity for ethyl acetate.
Adhesion of L. monocytogenes Scott A grown in TSYE at
different temperatures.
The numbers of culturable bacteria
adhering to stainless steel under the eight conditions studied here are
shown in Table 2. At the four growth
temperatures, bacterial cells bound more effectively to the stainless
steel when they were suspended in 1.5 × 101 M NaCl
than when they were suspended in 1.5 × 103 M NaCl
(P < 0.05). Furthermore, adhesion was greatest for
bacterial cells cultivated at 37°C and lowest for cells cultivated at
15°C (P < 0.05), and the number of attached bacteria
decreased between 20 and 15°C. A graph of the affinity of cells for
ethyl acetate as determined by the MATS method versus the number of
adherent cells in the presence of 1.5 × 103 M NaCl
at the four growth temperatures used is shown in Fig. 4. The linear coefficients of correlation
between bacterial affinity for ethyl acetate and bacterial adhesion to
stainless steel were 0.93 and 0.80 for adhesion assays performed in the
presence of 1.5 × 103 and 1.5 × 101 M NaCl, respectively.
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1 or 1.5 × 103 M NaCl, the viable
cell counts were not affected (P < 0.05).
The Lifshnitz-van der Waals, electron donor, and electron acceptor
components of the surface free energy of the stainless steel chips, as
determined by contact angle measurements, were 39, 13, and 0.3 mJ
· m2, respectively.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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The aim of this study was to investigate the influence of growth conditions (medium and temperature) on the physicochemical surface properties of L. monocytogenes Scott A. Microbial cell surfaces were found to be hydrophilic when bacteria were grown at 37°C in BHI medium or TSYE. However, the hydrophilicity decreased when microbial cells were cultivated in TSYE supplemented with either glucose or lactic acid. These findings are consistent with results obtained by Mafu et al. (28), who used the hydrophobic interaction chromatography technique and found that the hydrophobicity of L. monocytogenes Scott A increased as the pH decreased.
Furthermore, bacterial cells cultivated in BHI medium and bacterial cells cultivated in TSYE exhibited the same physicochemical differences when they were cultivated at different temperatures, and cells grown in media supplemented with glucose or lactic acid exhibited greater affinity with the electron donor solvent (ethyl acetate), which indicated that more electron acceptor groups were present on the cell wall. The presence of bound acidic compounds on the cell walls of the bacteria could explain this phenomenon. The low pH of a culture grown in a glucose-enriched medium in the stationary phase was undoubtedly related to the metabolism of glucose to lactic or acetic acid (38).
Under all of the growth conditions studied, L. monocytogenes
cells had a high negative charge, and the electrophoretic mobilities at
pH 7 were greater than the value (2.07 µm/V/cm/s) obtained for the
same strain by Mafu et al. (27). However, the storage conditions (4°C), growth medium (Trypticase soy broth supplemented with 1% yeast extract), and suspending medium (sodium phosphate buffer) were different in the study of Mafu et al.
Bacterial charge is attributed to cell wall constituents
(36) (e.g., phosphate, carboxylate groups, and proteins).
Progressive reductions in the electrophoretic mobility of cells as the
pH decreases are due to gradual increases in the protonation of several chemical groups. Our failure to determine the isoelectric points in the
pH range which we used (pH 2 to 7) indicates that compounds with very
low pKa were present on the cell surfaces. Considering the
composition of the L. monocytogenes cell wall
(42), the characteristics described above might be related
to the low pKa (pKa < 2.1) of the
phosphate groups in phosphodiester bridges (R-O-HPO2-O-R/R-O-PO2-O-R) of
cell wall teichoic acids (37).
The electrophoretic mobility of cells cultivated in either one of the supplemented media seemed to be less pH dependent, and the decrease in mobility was more subtle when the pH of the microbial suspension was reduced below pH 4. Supplementing the growth medium with glucose or lactic acid also reduced the electrophoretic mobility of the bacteria at pH values above 4 through direct neutralization of the negatively charged groups present on cell walls linked to a decrease in the pH of the medium.
The growth temperature had a significant nonlinear effect on the
electrophoretic mobility of L. monocytogenes Scott A cells grown in either TSYE or BHI medium. In particular, changes in electrophoretic mobility were observed between 15 and 8°C; at these
temperatures the values decreased dramatically and were less pH
dependent, and almost no changes were observed after the microbial
suspension was acidified. This difference in activity at low pH values
could have been due to differences in the nature of the negative charge
of the cells. The rapid reduction in electrophoretic mobility around pH
4 may indicate that protein- or peptidoglycan-associated COOH/COO (4 < pKa < 5) was
present on the cell walls (37). Hence, cells grown at 8°C
may have had fewer carboxyl groups than cells grown at the other
temperatures. Differences observed at this growth temperature may also
have been related to a glycolipid that was isolated from L. monocytogenes only after growth at a low temperature (23).
The high negative charge of bacterial cells at 15 and 20°C may have
been linked to the presence of temperature-dependent production of
flagella by L. monocytogenes. Many flagella were observed on cells grown at 20°C, whereas at 37°C very few flagella were
observed (35). The rich protein (and protein-associated
COOH/COO) content of flagella could explain the specific
electric properties of cells cultivated at 15 or 20°C. The
differences in physicochemical properties of cells grown in different
media and at different temperatures may also have reflected the
synthesis of acclimation proteins (6) due to acidic or
thermal stresses during bacterial growth, which could have led to
changes in cell wall composition.
Unlike van der Waals and Lewis acid-base interactions, electrostatic
interactions are inhibited in a high-ionic-strength suspending liquid.
The greatest adhesion of microbial cells in a high-ionic-strength suspending liquid (1.5 × 101 M NaCl) indicated that
there was electrostatic repulsion between the negatively charged
bacteria and the stainless steel. These results are consistent with
previously published data which indicated that the isoelectric point of
stainless steel was around pH 4 and varied slightly depending on the
surface finish and the cleaning treatments (9). The L. monocytogenes Scott A adhesion data correlated best with cell
affinity for ethyl acetate, which indicates the importance of Lewis
acid-base interactions for cell adhesion to stainless steel. This
correlation is consistent with the physicochemical characteristics of
ethyl acetate and stainless steel, both of which have strong electron
donor surface properties and weak electron acceptor characteristics.
Hence, our data suggest that both electrical and Lewis acid-base
interactions are involved in L. monocytogenes Scott A
adhesion to stainless steel. The influence of lactic acid in the growth
medium on the adhesion of L. monocytogenes to stainless steel has been described previously (10). Variations in cell hydrophobicity caused by lactic acid led to significant variations in
the adherent bacteria, implying that van der Waals interactions play a
role in cell adhesion. Therefore, the growth conditions can influence
the various components of microbial cell surface physicochemical
properties (electrostatic, Lewis acid-base, and van der Waals
interactions) and, consequently, the adhesion of cells to surfaces.
Recently, Andersson et al. found that there is a relationship among
Bacillus cereus spore adhesion to epithelial cells, surface
hydrophobicity, and the virulence of strains (3). Adhesion
assays performed with different surfaces that are representative of
plants or epithelial cells and with L. monocytogenes strains whose pathogenicity is known are needed to improve our understanding of
the relationships between physicochemical properties of microbial cells
and pathogenicity.
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ACKNOWLEDGMENTS |
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This work was supported by the UNIR (Ultrapropre Nutrition Industrie Recherche) program, which involves food companies, the French Ministry of Agriculture, and the French Ministry of Research.
We thank Michael Dever and Dipak Sarker for revising the English in the manuscript.
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FOOTNOTES |
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* Corresponding author. Mailing address: INRA UBHM, 25 Avenue République, 91300 Massy, France. Phone: 33 1 69 53 64 00. Fax: 33 1 60 13 36 01. E-mail: briandet{at}massy.inra.fr.
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REFERENCES |
|---|
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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| 1. | Ahamad, N., and E. H. Marth. 1989. Behavior of Listeria monocytogenes at 7, 13, 21, and 35°C in tryptose broth acidified with acetic, citric, or lactic acid. J. Food Prot. 52:688-695. |
| 2. |
Al-Makhlafi, H.
1994.
Influence of preadsorbed milk proteins on adhesion of Listeria monocytogenes to hydrophobic and hydrophilic silica surfaces.
Appl. Environ. Microbiol.
60:3560-3565 |
| 3. | Andersson, A., P. E. Granum, and U. Rönner. 1998. The adhesion of Bacillus cereus spores to epithelial cells might be an additional virulence mechanism. Int. J. Food Microbiol. 39:93-99[Medline]. |
| 4. |
Baloga, A. O., and S. K. Harlander.
1991.
Comparison of methods for discrimination between strains of Listeria monocytogenes from epidemiological surveys.
Appl. Environ. Microbiol.
57:2324-2331 |
| 5. | Barbosa, W. B., L. Cabedo, H. J. Wederquist, J. N. Sofos, and G. R. Schmidt. 1994. Growth variation among species and strains of Listeria in culture broth. J. Food Prot. 57:765-775. |
| 6. | Bayles, D. O., B. A. Annous, and B. J. Wilkinson. 1996. Cold stress proteins induced in Listeria monocytogenes in response to temperature downshock and growth at low temperatures. Appl. Environ. Microbiol. 62:1116-1119[Abstract]. |
| 7. | Begot, C., I. Lebert, and A. Lebert. 1997. Variability of the response of 66 Listeria monocytogenes and Listeria innocua strains to different growth conditions. Food Microbiol. 14:403-412. |
| 8. | Bellon-Fontaine, M. N., J. Rault, and C. J. van Oss. 1996. Microbial adhesion to solvents: a novel method to determine the electron-donor/electron-acceptor or Lewis acid-base properties of microbial cells. Colloids Surfaces B Biointerfaces 7:47-53. |
| 9. | Boulangé-Petermann, L., A. Doren, B. Baroux, and M. N. Bellon-Fontaine. 1995. Zeta potential measurements on passive metals. J. Colloid Interface Sci. 171:179-186. |
| 10. | Briandet, R., V. Leriche, B. Carpentier, and M. N. Bellon-Fontaine. 1999. Effects of the growth conditions on the surface hydrophobicity of Listeria monocytogenes cells and their adhesion to stainless steel. J. Food Prot. 62:994-998[Medline]. |
| 11. | Briandet, R., E. K. Kemsley, and R. H. Wilson. 1996. Approaches to adulteration detection in instant coffees using infrared spectroscopy and chemometrics. J. Sci. Food Agric. 71:359-366. |
| 12. | Buchanan, R. L., H. G. Stahl, and R. C. Whiting. 1989. Effects and interactions of temperature, pH, atmosphere, sodium chloride, and sodium nitrite on the growth of Listeria monocytogenes. J. Food Prot. 52:844-851. |
| 13. | Buchanan, R. L., and J. G. Phillips. 1990. Response surface model for predicting the effects of temperature, pH, sodium chloride content, sodium nitrite concentration and atmosphere on the growth of Listeria monocytogenes. J. Food Prot. 53:370-376. |
| 14. | Buncic, S., and S. M. Avery. 1996. Relationship between variations in pathogenicity and lag phase at 37°C of Listeria monocytogenes previously stored at 4°C. Lett. Appl. Microbiol. 23:18-22[Medline]. |
| 15. |
Dickson, J. S., and M. Koohmaraie.
1989.
Cell surface charge characteristics and their relationship to bacterial attachment to meat surfaces.
Appl. Environ. Microbiol.
55:832-836 |
| 16. | Duffy, G., and J. J. Sheridan. 1997. The effect of temperature, pH and medium in a surface adhesion immunofluorescent technique for detection of Listeria monocytogenes. J. Appl. Microbiol. 83:95-101[Medline]. |
| 17. |
Farber, J. M., and P. I. Peterkin.
1991.
Listeria monocytogenes, a food-borne pathogen.
Microbiol. Rev.
55:476-511 |
| 18. |
Fleming, J. M.,
S. L. Cochi,
K. L. MacDonald,
J. Brondum,
P. S. Hayes,
B. D. Plikaytis,
M. B. Holmes,
A. Audurier,
C. V. Broome, and A. L. Reingold.
1985.
Pasteurized milk as a vehicle of infection in an outbreak of listeriolisis.
N. Engl. J. Med.
312:404-407 |
| 19. | Geertsema-Doornbush, G. I., H. C. Van der Mei, and H. J. Bussher. 1993. Microbial cell surface hydrophobicity: the involvement of electrostatic interactions in microbial adhesion to hydrocarbons (MATH). J. Microbiol. Methods 18:61-68. |
| 20. | George, S. M., B. M. Lund, and T. F. Brocklehurst. 1988. The effect of pH and temperature on initiation of growth of Listeria monocytogenes. Lett. Appl. Microbiol. 6:153-156. |
| 21. | Horska, E., J. Pokorny, and M. Labajova. 1993. Changes of surface charge and hydrophobicity of the outer bacterial membrane depending on the cultivation medium. Biologia (Bratislava) 48:343-347. |
| 22. | Ita, P. S., and R. W. Hutkins. 1991. Intracellular pH and survival of Listeria monocytogenes Scott A in tryptic soy broth containing acetic, lactic, citric, and hydrochloric acids. J. Food Prot. 54:15-19. |
| 23. | Jones, C. E., G. Shama, D. Jones, I. S. Roberts, and P. W. Andrew. 1997. Physiological and biochemical studies on psychrotolerance in Listeria monocytogenes. J. Appl. Microbiol. 83:31-35[Medline]. |
| 24. | Kim, K. Y., and J. F. Frank. 1994. Effect of growth nutrients on attachment of Listeria monocytogenes to stainless steel. J. Food Prot. 57:720-726. |
| 25. | Kim, K. Y., and J. F. Frank. 1995. Effect of nutrients on biofilm formation by Listeria monocytogenes on stainless steel. J. Food Prot. 58:24-28. |
| 26. | Kouassi, Y., and L. A. Shelef. 1996. Metabolic activities of Listeria monocytogenes in the presence of sodium propionate, acetate, lactate and citrate. J. Appl. Bacteriol. 81:147-153[Medline]. |
| 27. | Mafu, A. A., D. Roy, J. Goulet, and P. Magny. 1990. Attachment of Listeria monocytogenes to stainless steel, glass, polypropylene, and rubber surfaces after short contact times. J. Food Prot. 53:742-746. |
| 28. |
Mafu, A. A.,
D. Roy,
J. Goulet, and L. Savoie.
1991.
Characterization of physicochemical forces involved in adhesion of Listeria monocytogenes to surfaces.
Appl. Environ. Microbiol.
57:1969-1973 |
| 29. | McClure, P. J., A. L. Beaumont, J. P. Sutherland, and T. A. Roberts. 1996. Predictive modelling of growth of Listeria monocytogenes. The effects on growth of NaCl, pH, storage temperature and NaNO2. Int. J. Food Microbiol. 34:221-232. |
| 30. | McLauchlin, J., A. M. Tidley, and A. G. Taylor. 1989. The use of monoclonal antibodies against Listeria monocytogenes in a direct immunofluorescence technique for the rapid presumptive identification and direct demonstration of Listeria in food. Acta Microbiol. Hung. 36:467-471[Medline]. |
| 31. | Oh, D.-H., and D. L. Marshall. 1993. Influence of temperature, pH, and glycerol monolaurate on growth and survival of Listeria monocytogenes. J. Food Prot. 56:744-749. |
| 32. | Palumbo, S. A., and A. C. Williams. 1990. Effect of temperature, relative humidity, and suspending menstrue on the resistance of Listeria monocytogenes to drying. J. Food Prot. 53:377-381. |
| 33. | Papageorgiou, D. K., and E. H. Marth. 1989. Behaviour of Listeria monocytogenes at 4 and 22°C in whey and skim milk containing 6 or 12% sodium chloride. J. Food Prot. 52:625-630. |
| 34. | Patchett, R. A., N. Watson, P. S. Fernandez, and R. G. Kroll. 1996. The effect of temperature and growth rate on the susceptibility of Listeria monocytogenes to environmental stress conditions. Appl. Microbiol. 22:121-124. |
| 35. |
Peel, M.,
W. Donachie, and A. Shaw.
1988.
Temperature-dependent expression of flagella of Listeria monocytogenes studied by electron microscopy, SDS-PAGE and Western blotting.
J. Gen. Microbiol.
134:2171-2178 |
| 36. | Pelletier, C., C. Bouley, C. Cayvela, S. Boutier, P. Bourlioux, and M. N. Bellon-Fontaine. 1997. Cell surface characteristics of Lactobacillus casei subsp. casei, Lactobacillus paracasei subsp. paracasei, and Lactobacillus rhamnosus strains. Appl. Environ. Microbiol. 63:1725-1731[Abstract]. |
| 37. | Rijnaarts, H. H. M., W. Norbe, J. Lyklema, and A. J. B. Zehnder. 1995. The isoelectric point of bacteria as an indicator for the presence of cell surface polymers that inhibit adhesion. Colloids Surf. B Biointerfaces 4:191-197. |
| 38. | Romick, T. L., and H. P. Fleming. 1998. Acetoin production as an indicator of growth and metabolic inhibition of Listeria monocytogenes. J. Appl. Microbiol. 84:18-24. |
| 39. | Rosenow, E. M., and E. H. Marth. 1987. Growth of Listeria monocytogenes in skim, whole and chocolate milk, and in whipping cream during incubation at 4, 8, 13, 21 and 35°C. J. Food Prot. 50:452-459. |
| 40. |
Roy, B.,
H. W. Ackermann,
S. Pandian,
G. Picard, and G. Goulet.
1993.
Biological inactivation of adhering Listeria monocytogenes by listeria phages and a quaternary ammonium compound.
Appl. Environ. Microbiol.
59:2914-2917 |
| 41. | Sasahara, K. C., and E. A. Zottola. 1993. Biofilm formation by Listeria monocytogenes utilizes a primary colonizing microorganism in flowing systems. J. Food Prot. 56:1022-1028. |
| 42. | Seeliger, H. P. R., and D. Jones. 1986. Listeria, p. 1235-1244. 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 |
| 43. | Sorrells, K. M., D. C. Enigl, and J. R. Hatfield. 1989. Effect of pH, acidulant, time, and temperature on the growth and survival of Listeria monocytogenes. J. Food Prot. 52:571-573. |
| 44. | Stephens, J. C., I. S. Roberts, D. Jones, and P. W. Andrew. 1991. Effect of growth temperature on virulence of strains of Listeria monocytogenes in the mouse: evidence for a dose dependence. J. Appl. Bacteriol. 70:239-244[Medline]. |
| 45. |
van Loosdrecht, M. C. M.,
J. Lyklema,
W. Norde,
G. Schraa, and A. J. B. Zehnder.
1987.
The role of bacterial cell wall hydrophobicity in adhesion.
Appl. Environ. Microbiol.
53:1893-1897 |
| 46. | van Oss, C. J., M. K. Chaudhury, and R. J. Good. 1988. Interfacial Lifshitz-van der Waals and polar interactions in macroscopic systems. Chem. Rev. 88:927-941. |
| 47. | van Oss, C. J. 1993. Acid-base interfacial interactions in aqueous media. Colloids Surf. A Physicochem. Eng. Aspects 78:1-49. |
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