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Applied and Environmental Microbiology, July 2008, p. 4543-4549, Vol. 74, No. 14
0099-2240/08/$08.00+0     doi:10.1128/AEM.02041-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Coordinated Regulation of Cold-Induced Changes in Fatty Acids with Cardiolipin and Phosphatidylglycerol Composition among Phospholipid Species for the Food Pathogen Listeria monocytogenes{triangledown},{dagger}

S. K. Mastronicolis,1* N. Arvanitis,1 A. Karaliota,2 P. Magiatis,3 G. Heropoulos,4 C. Litos,2 H. Moustaka,1 A. Tsakirakis,1 E. Paramera,1 and P. Papastavrou1

Food Chemistry Laboratory,1 Inorganic Chemistry Laboratory, Chemistry Department,2 Laboratory of Pharmacognosy and Natural Products Chemistry, Faculty of Pharmacy, University of Athens, Panepistimiopolis Zografou 15771, Athens, Greece,3 National Hellenic Research Foundation, Institute of Organic and Pharmaceutical Chemistry, 48 Vas. Constantinou Ave., Athens, Greece4

Received 6 September 2007/ Accepted 14 May 2008


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ABSTRACT
 
We present here the structural identification of four phospholipid (Phl) classes in Listeria monocytogenes, the fatty acid (FA) composition for each individual Phl species, and a description of cold-induced FA changes. Cardiolipin (48.5%) and phosphatidylglycerol (18.1%) are dominated by anteiso-FA, and the previously recognized branched FA chain shortening by cold was observed singularly in these Phls. Phosploaminolipid (19.9%) and phosphatidylinositol, (9.1%) are significantly different, containing significant amounts of straight-chain FA. These findings are supported by nuclear magnetic resonance analysis.


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INTRODUCTION
 
The bacterium Listeria monocytogenes, one of the leading causes of food-borne illness (15), can adapt to cold and salinity (9, 10, 31, 46, 53) and can survive even on dust or flakes of organic material (34). Listeria is characterized by >85% branched-chain fatty acids (FA), anteiso-15:0 (a-15:0) and anteiso-17:0 (a-17:0). Cells grown in the cold (5°C) contain significantly less a-17:0 than those grown at higher temperatures (4, 8, 37, 43, 44, 57). A cryotolerance element of Listeria is also its ability to use cryoprotectant osmolytes (31), a property shared by other organisms (2, 3, 12, 21, 23). The critical role of odd numbered anteiso-FA in influencing the lower-temperature growth limits has recently been reported (14, 19, 25). We have reported previously (39) that Listeria spp. can be cold adapted by an increased content (30%) of neutral lipids (NL) among total lipids (TL) and an increase in the a-15:0/a-17:0 FA ratio (FAr) of TL, polar lipids (PL), and NL (10-, 10-, and 7-fold, respectively), as well as by an increase in FAr (38) for each NL subclasses 1,2-diglyceride, 1,3-diglyceride and free FA (6-, 5-, and 8-fold, respectively).

This study is a continuation (35, 36) of an investigation for the structural characterization of the major phospholipid (Phl) classes of L. monocytogenes, in order to (i) elucidate the isolation and quantification of each of class (cells at 30°C), (ii) evaluate the cold temperature (5°C) effect on each individual Phl class FA composition, and (iii) confirm the findings by 1H-nuclear magnetic resonance (NMR) analysis.

An avirulent strain of L. monocytogenes, DP-L1044 (D. Portnoy, University of Pennsylvania), prepared by a transposon insertion (6) in the parent strain (Lm10403S), was grown in brain heart infusion (Difco Laboratories) broth at 30°C (ca. 24 h). A 10-ml portion of this was then inoculated in 1 liter of brain heart infusion broth, followed by incubation until stationary phase (30 or 5°C). Cells pelleted by centrifugation were washed twice in phosphate buffer (pH 7.0). TL were extracted (17) and separated to PL and NL by solid-phase extraction (SPE) as previously described (38). Solvent A (chloroform-methanol-acetic acid-water [50:25:6:2,vol/vol/vol/vol]) was used for one-dimensionalal thin-layer chromatography (1D-TLC; silica gel G60 aluminum chromatoplate [Merck 1.05554], 0.25-mm thick, 10 by 10 cm). Spots were visualized by using iodine, ninhydrin, phosphomolybdenum blue (13), and copper sulfate (5, 42). Glyco- or sulfolipids were tested by using naphtholsulfuric acid (24). The standards phosphatidic acid (PA), phosphatidylserine (PS), cardiolipin (CL), phosphatidylglycerol (PG), phosphatidylethanolamine (PE), phosphatidylcholine (PC), phosphatidylinositol (PI), Lyso-PC, and Lyso-PE were purchased from Sigma Chemical Co. Each culture 30°C or 5°C PL sample (85 and 50 µg of phosphorus correspondingly) was fractionated by 1D-TLC (preparative), along with the standards (CL, PG, and PI) and along with another Listeria PL sample (30°C) aliquot (3.5 µg of phosphorus) as an alternative standard. Four individual Phl bands were separated, scraped off, and eluted from silica gel as previously described (35, 39). Each extracted band of residual lipids was used for analytical methods and 1H-NMR spectroscopy.

Total phosphorus (33), esters (47), nitrogen (20), and glycerol (30) analysis was performed as described previously. Deacylation (27, 54) was also performed in 0.1 ml of NaOH (1.2 N) in 50% (vol/vol) methanol at 45°C for 20 min. The PL in bulk were quantitated by weight after SPE column elution. Each individual Phl band (cells 30°C) was quantified after 1D-TLC fractionation of the PL sample (~10 µg of phosphorus) with solvent A (n = 10). Each iodine-visualized band was scraped into a digestion tube, and the total phosphorus content was determined (27). A 25-µg phosphorus sample of the TLC-extracted CL band (cells of 30°C) was dry acid methanolysed (51) by 400 µl of 3 N methanolic HCl, and the molecular ratios (structural data) were determined in hydrolysis aliquots as described previously (28).

For each culture CL, PG, phosphoaminolipids (PhAL), and PI FA were methylated by scraping the 1D-TLC bands into digestion tubes, and a 1-mg PL sample was also methylated as previously described (28, 35). FA methyl esters were separated by using a Hewlett-Packard 6890 gas chromatograph with split/splitless injector, flame ionization detector (30 m by 0.251 mm, capillary column DB-5ms; J&W Scientific). The carrier gas was He. The injector and detector were maintained at 250 and 280°C, respectively. The oven temperature was ramped from 90 to 170°C (70°C/min) and from 170 to 210°C (5°C/min). The initial and final holding times were 1 and 2 min, respectively. Two standards were used: bacterial FA methyl esters (CP Matreya, Inc.) and marine oil fame (Restek Corp.). Each lipid sample was analyzed by gas chromatography-mass spectrometry (electron impact or chemical ionization with acetonitrile) using a Varian Saturn 2000 with a 30-m-by-0.25-mm DB5-ms column. To each sample of CL (750 µg), PG (270 µg), PhAL (270 µg), and PI (150 µg) 0.5 ml of CDCl3/CD3OD (1:2 [vol/vol]) was added, and 1H-NMR spectra were acquired by using a Varian Unity Plus spectrometer (300 MHz). As standards, CL (1,000 µg), PG (540 µg), and PI (920 µg) were also analyzed.

L. monocytogenes TL extraction (at 30 or 5°C) yielded 5.2 ± 1.2 mg g–1 and 6.5 ± 1.4 mg g–1 wet cells. The TL lipid phosphorus and nitrogen contents were 3.4% ± 0.2% (30°C) and 2.5% ± 0.1% (5°C) and 0.96% ± 0.02% and 0.86% ± 0.02%, respectively. The PL for each culture represented 62.5% ± 2.3% and 53.3% ± 1.1%, respectively, of the TL. PL were separated by 1D-TLC into four phosphocomponents (see Fig. S1 in the supplemental material) designated g, f, e, and b, as we have previously described (36) for Listeria (30°C). Two bands, f and b, were cochromatographed with PG and PI standards, respectively. The component f includes (after 2D-TLC separation) two phosphocomponents, f2 and f3, but not the glycocomponent f1 (35). The component g was cochromatographed close to the CL standard. The ninhydrin-positive phosphocomponent e (migrated just below the PG position) is the single PhAL of Listeria (35, 36), as others (16) have also reported, and a lysylcardiolipin structure is suggested. This molecule can serve as a genus-specific chemotaxonomic marker for the genus Listeria. Table 1 shows the lipid phosphorus distribution of each lipid component (cells at 30°C). Of note is that the ratio of relative amounts at phosphorus percentages for CL/PhAL (~2.4) are similar to that (~2.8) reported by Fischer and Leopold (16). The existence of CL and PG has been reported by others (16, 32). Until now there has been no precedent in the literature for the existence of PI in Listeria PL.


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  		TABLE 1. Separation and composition (% of lipid P) of L. monocytogenes PLa from cell cultures at 30°C

Based on their TLC behavior before and after deacylation, the four phosphocomponents of each culture PL sample were completely hydrolyzed, and the bulk of the lipid phosphorus was distributed in the water-soluble products. This suggests a basic glycerolipid structure for each phosphocomponent. The hydrolysis products after dry acid methanolysis of the phosphocomponent g, contained total phosphorus, (methyl) esters, and glycerol at a molar ratio of 2.00:4.00:3.12, respectively, and this suggests a diphosphatidylglycerol (cardiolipin) molecular structure.

The four isolated glycerolipid components were also identified by 1H-NMR analysis (Tables 2 and 3). For each lipid class, the spectral assignments were compared to standard spectra of CL, PI, and PG (1, 7, 48). Diagnostic resonances may be considered to be the CL resonances of the central glycerol head group, sandwiched between two phosphate groups (OPCH2CHOHCH2OP) (Table 3 and Fig. 1) and, in principle, the PG resonances of its glycerol head group C4H2C5HC6H2 (Table 3 and Fig. 2). The PI head group is complicated because it represents a network of six interacting spins corresponding to the six inositol CH protons (see Fig. S3 in the supplemental material). The three features distinguishing PI are the C-4(POCH), C-6(CHOH), and C-7(CHOH) proton resonances (Table 3). The C-8(CHOH) signal at 3.200 ppm is overlapped by the methanol resonance. C-5 has the same peak (4.341ppm) as glycerol backbone C-1 (1, 7). The PhAL head group is suggested to be the same as the CL headgroup, with an esterified lysine moiety at the central free OH group. The methylene protons neighboring the {varepsilon}-amino group of lysine (CH2NH2) occur at 3.001 ppm. The central glycerol sandwiched between two phosphate groups could also be used as a diagnostic for this lipid (see Fig. S2 in the supplemental material) as for the CL structure described above.


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  		TABLE 2. Comparison of 1H chemical shifts for different lipid glycerol backbonesa


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  		TABLE 3. Comparison of 1H chemical shifts for different lipid head groupsa


Figure 1
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  		FIG. 1. 1H-NMR spectra of L. monocytogenes cardiolipin class, extracted from preparative TLC, from cultures at 30°C (down) and 5°C (up). For samples, the solvent CDCl3/CD3OD (1:2 [vol/vol]) was used.


Figure 2
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  		FIG. 2. 1H-NMR spectra of L. monocytogenes phosphatidylglycerol class, extracted from preparative TLC, from a culture at 30°C. For samples, the solvent CDCl3/CD3OD (1:2 [vol/vol]) was used.

This study represents the individual isolated Phl species (CL, PG, PhAL, and PI) FA composition of Listeria (30°C). FA profiles of CL and PG are very similar and dominated by anteiso-FA. The PhAL and PI FA compositions are significantly different, containing significant amounts of straight-chain FA (16:0 and 18:0) and unsaturated FA (Table 4).


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  		TABLE 4. Cold temperature dependence of FA composition (wt %) of CL, PG, PhAL, and PI from two sets of L. monocytogenes cultures at 30 and 5°Ca

Upon cold stress the a-15:0 FA proportion in their CL and PG of Listeria increased dramatically (Table 4). The main cold change for PhAL FA was, apart from the increase of anteiso-15:0, the decrease of the sum of unsaturated FA. Cold differences between the FA composition of PI species (unpublished data) were mainly independent of the growth temperature (the differences varied between ±4.0 percentage points, with the exception of a 15:0 FA, which showed a difference of +6.2). Conclusively, the cold metabolic change in CL and PG is different from the rest of the PL subclasses (PI and PhAL). The cold decrease of the -CH2-/-CH3 ratio of the acyl chains by NMR analysis (Table 5 and Fig. 3) reflects the cold increase of the branched-15:0/branched-17:0 FA ratio (as determined by gas chromatography analysis) for CL and PG, as well as for PhAL (Table 4). The determination of branched FA by 1H-NMR analysis can be a useful interpretation tool of FA microorganism metabolism at cold temperature.


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  		TABLE 5. Temperature dependence of the -CH2-/-CH3 ratio of CL, PG, and PhAL FA chains from cells of L. monocytogenes grown at 30 and 5°Ca


Figure 3
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  		FIG. 3. 1H-NMR spectra (acyl chains only) of L. monocytogenes cardiolipin (A) and phosphatidylglycerol (B) extracted from preparative TLC, from cultures at 30°C (down) and 5°C (up). For samples, the solvent CDCl3/CD3OD (1:2 [vol/vol]) was used.

The potential impacts of studying L. monocytogenes membrane Phl composition are that (i) molecules can serve as a chemotaxonomic marker, (ii) resistance to antimicrobials and nisin (11, 40, 41, 52, 56) or other antimicrobial peptides (49, 50) is correlated with both altered FA composition (26) and Phl compositional changes, (iii) antibacterials encapsulated in liposomes produced with PhL of similar structure as that included in Listeria membrane are more effective (improved permeation) (55), (iv) an understanding of the cold stress response ia helpful in the design of effective food preservation strategies (such as membrane-disrupting techniques like pulsed electric fields, ultrahigh pressure, etc.) applicable to hurdle technology, etc. (45), and (v) FA biosynthesis is coordinately regulated with Phl synthesis and growth as part of the bacteria response to the changing environment and offers unique sites for selective inhibition (22) to combat microbial infection (chemotherapeutic agents). Phl FA fingerprints help us to monitor the impact on bacterial growth conditions (18).


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ACKNOWLEDGMENTS
 
This research was supported in part by the Special Research Account of National and Kapodistrian University of Athens under project no. 70/4/3338.


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FOOTNOTES
 
* Corresponding author. Mailing address: Food Chemistry Laboratory, Department of Chemistry, Panepistimiopolis Zografou 15771, Athens, Greece. Phone: 30 210 7274326. Fax: 30 210 7274476. E-mail: smastro{at}chem.uoa.gr Back

{triangledown} Published ahead of print on 23 May 2008. Back

{dagger} Supplemental material for this article may be found at http://aem.asm.org/. Back


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REFERENCES
 
    1
  1. Adosraku, R. K., J. D. Smith, and A. Nicolaou. 1996. Tetrahymena thermophila: analysis of phospholipids and phosphonolipids by high-field 1H-NMR. Biochim. Biophys. Acta 1299:167-174.[Medline]
    2. 2
  2. Angelidis, A. S., L. T. Smith, and G. M. Smith. 2002. Elevated carnitine accumulation by Listeria monocytogenes impaired in glycine betaine transport is insufficient to restore wild-type cryotolerance in milk whey. Int. J. Food Microbiol. 75:1-9.[CrossRef][Medline]
    3. 3
  3. Angelidis, A. S., and G. M. Smith. 2003. Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium. Appl. Environ. Microbiol. 69:7492-7498.[Abstract/Free Full Text]
    4. 4
  4. 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 temperatures. Appl. Environ. Microbiol. 69:3887-3894.
    5. 5
  5. Bhat, H. K., and A. S. Ansari. 1989. Improved separation of lipid esters by thin-layer chromatography. J. Chromatogr. 483:369-378.[CrossRef][Medline]
    6. 6
  6. Camilli, A., H. Goldfine, and D. A. Portnoy. 1991. L. monocytogenes mutants lacking phosphatidylinositol specific phospholipase C are avirulent. J. Exp. Med. 173:751-754.[Abstract/Free Full Text]
    7. 7
  7. Casu, M., G. J. Anderson, G. Choi, and W. A. Gibons. 1991. NMR lipid profiles of cells, tissues and body fluids. Magn. Res. Chem. 29:594-602.[CrossRef]
    8. 8
  8. Chihib, N. E., M. Ribeiro da Silva, G. Delattre, M. Laroche, and M. Federighi. 2003. Different cellular fatty acid pattern behaviors of two strains of Listeria monocytogenes Scott A and CNL 895807 under different temperature and salinity conditions. FEMS Microbiol. Lett. 218:155-160.[CrossRef][Medline]
    9. 9
  9. Cole, M., M. Jones, and C. Holyoak. 1990. The effect of pH, salt concentration, and temperature on the survival and growth of Listeria monocytogenes. J. Appl. Microbiol. 69:63-72.[Medline]
    10. 10
  10. Conner, D. E., R. E. Brackett, and L. R. Beuchat. 1986. Effect of temperature, sodium chloride, and pH on growth of Listeria monocytogenes in cabbage juice. Appl. Environ. Microbiol. 52:59-63.[Abstract/Free Full Text]
    11. 11
  11. Crandall, A. D., and T. J. Montville. 1998. Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype. Appl. Environ. Microbiol. 64:231-237.[Abstract/Free Full Text]
    12. 12
  12. Deshnium, P., Z. Gombos, Y. Nishiyama, and N. Murata. 1997. The action in vivo of glycine betaine in enhancement of tolerance of Synechococcus sp. strain PCC 7942 to low temperature. J. Bacteriol. 179:339-344.[Abstract/Free Full Text]
    13. 13
  13. Dittmer, J. C., and R. L. Lester. 1964. A simple specific spray for the detection of phospholipids on thin-layer chromatography. J. Lipid Res. 5:126-127.
    14. 14
  14. Edgcomb, M. R., S. Sirimanne, B. J. Wilkinson, P. Drouin, and P. D. Morse II. 2000. Electron paramagnetic resonance studies of the membrane fluidity of the food-borne pathogenic psychrotroph Listeria monocytogenes. Biochim. Biophys. Acta 1463:31-42.[Medline]
    15. 15
  15. Farber, J. M., and P. I. Peterkin. 2000. Listeria monocytogenes. Microbiol. Safety Quality 2000:1178-1232.
    16. 16
  16. Fischer, W., and K. Leopold. 1999. Polar lipids of four Listeria species containing L-lysylcardiolipin, a novel lipid structure and other unique phospholipids. Int. J. Syst. Bacteriol. 49:653-662.[Abstract/Free Full Text]
    17. 17
  17. Folch, J., M. Lees, and G. H. Stanley-Sloane. 1957. A simple method for the isolation and purification of total-lipids from animal tissues. J. Biol. Chem. 226:497-509.[Free Full Text]
    18. 18
  18. Fouchard, S., Z. Abdellaouni-Maane, A. Boulanger, P. Llopiz, and S. Neunlist. 2005. Influence of growth conditions on Pseudomonas fluoerescens strains: a link between metabolite production and the PLFA profile. FEMS Microbiol. Lett. 251:211-218.[CrossRef][Medline]
    19. 19
  19. Gerhardt, P. N. M., L. T. Smith, and G. M. Smith. 2000. Osmotic and chill activation of glycine betaine porter II in Listeria monocytogenes membrane vesicles. J. Bacteriol. 182:2544-2550.[Abstract/Free Full Text]
    20. 20
  20. Hashmi, M. H., E. Ali, and M. Umar. 1962. Kjeldahl determination of nitrogen without distillation. Anal. Chem. 34:988-990.
    21. 21
  21. Hayashi, H., Alia, L. Mustardy, P. Deshnium, M. Ida, and N. Murata. 1997. Transformation of Arabidopsis thaliana with the cod A gene for choline oxidase; accumulation of glycine betaine and enhanced tolerance to salt and cold stress. Plant J. 12:133-142.[CrossRef][Medline]
    22. 22
  22. Heath, R. J., S. W. White, and C. O. Rock. 2001. Lipid biosynthesis as a target for antibacterial agents. Prog. Lipid Res. 40:467-497.[CrossRef][Medline]
    23. 23
  23. Holmstrom, K. O., S. Somersalo, A. Mandal, T. E. Palva, and B. Welin. 2000. Improved tolerance to salinity and low temperature in transgenic tobacco producing glucine betaine. J. Exp. Bot. 51:177-185.[Abstract/Free Full Text]
    24. 24
  24. Jacin, H., and A. R. Mishkin. 1965. Separation of carbohydrates on borate-impregnated silica gel G plates. J. Chromatogr. 18:170-173.[Medline]
    25. 25
  25. Jones, S. L., P. Drouin, B. J. Wilkinson, and P. D. Morse II. 2002. Correlation of long-range membrane order with temperature-dependent growth characteristics of parent and a cold-sensitive, branched-chain-fatty-acid-deficient of Listeria monocytogenes. Arch. Microbiol. 177:217-222.[CrossRef][Medline]
    26. 26
  26. Juneja, V. K., and P. M. Davidson. 1993. Influence of altered fatty acid composition of Listeria monocytogenes to antimicrobials. J. Food Prot. 56:302-305.
    27. 27
  27. Kariotoglou, D. M., and S. K. Mastronicolis. 1998. Phosphonolipids in the mussel Mytilus galloprovincialis. Z. Naturforsch. 53c:888-896.
    28. 28
  28. Kariotoglou, D. M., and S. K. Mastronicolis. 2001. Sphingophosphonolipids, phospholipids, and fatty acids from Aegean jellyfish Aurelia aurita. Lipids 36:1255-1264.[CrossRef][Medline]
    29. 29
  29. Kariotoglou, D. M., and S. K. Mastronicolis. 2003. Sphingophosphonolipid molecular species from edible mollusks and a jellyfish. CBP B Biochem. Mol. Biol. 136:27-44.[CrossRef]
    30. 30
  30. Kates, M. 1993. General analytical procedures in techniques of lipidology, p. 140-141. Elsevier, Oxford, United Kingdom.
    31. 31
  31. 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]
    32. 32
  32. Kosaric, N., and K. K. Carroll. 1971. Phospholipids of Listeria monocytogenes. Biochim. Biophys. Acta 239:428-442.[Medline]
    33. 33
  33. Long, C., and D. A. Staples. 1961. Chromatographic separation of brain lipids cerebroside and sulphatide. Biotechnol. J. 78:179-185.
    34. 34
  34. Marth, E. H. 1988. Disease characteristics of Listeria monocytogenes. Food Technol. 42:165-168.
    35. 35
  35. Mastronicolis, S. K., J. B. German, and G. M. Smith. 1996. Diversity of the polar lipids of the food-borne pathogen Listeria monocytogenes. Lipids 31:635-640.[Medline]
    36. 36
  36. Mastronicolis, S. K., J. B. German, and G. M. Smith. 1996. Isolation and fatty acid analysis of neutral and polar lipids of the food bacterium Listeria monocytogenes. Food Chem. 57:451-456.[CrossRef]
    37. 37
  37. Mastronicolis, S. K., J. B. German, N. Megoulas, E. Petrou, P. Foka, and G. M Smith. 1998. Influence of cold shock on the fatty-acid composition of different lipid classes of the food-borne pathogen Listeria monocytogenes. Food Microbiol. 15:299-306.[CrossRef]
    38. 38
  38. Mastronicolis, S. K., N. Arvanitis, A. Karaliota, C. Litos, G. Stavroulakis, H. Moustaka, A. Tsakirakis, and G. Heropoulos. 2005. Cold dependence of fatty acid profile of different lipid structures of Listeria monocytogenes. Food Microbiol. 22:213-219.[CrossRef]
    39. 39
  39. Mastronicolis, S. K., A. Boura, A. Karaliota, P. Magiatis, N. Arvanitis, C. Litos, A. Tsakirakis, P. Paraskevas, H. Moustaka, and G. Heropoulos. 2006. Effect of cold temperature on the composition of different lipid classes of the foodborne pathogen Listeria monocytogenes: focus on neutral lipids. Food Microbiol. 23:184-194.[CrossRef][Medline]
    40. 40
  40. Mazzotta, A. S., and T. J. Montville. 1997. Nisin induces changes in membrane fatty acid composition of Listeria monocytogenes nisin resistant strains at 10°C and 30°C. J. Appl. Microbiol. 82:32-38.[Medline]
    41. 41
  41. Ming, X., and M. A. Daeschel. 1995. Correlation of cellular phospholipid content with nisin resistance of Listeria monocytogenes Scott A. J. Food Protect. 58:416-420.
    42. 42
  42. Pucsok, J., L. Kovacs, A. Zalka, and R. Dobo. 1988. Separation of lipids by new thin-layer chromatography and over-pressured thin-layer chromatograph methods. Clin. Biochem. 21:81-85.[CrossRef][Medline]
    43. 43
  43. Puttmann, M., N. Ade, and H. Hof. 1993. Dependence of fatty acid composition of Listeria spp. on growth temperature. Res. Microbiol. 144:279-283.[Medline]
    44. 44
  44. Raines, L. J., C. W. Moss, D. Farshtchi, and B. Pittmann. 1968. Fatty acids of Listeria monocytogenes. J. Bacteriol. 96:2175-2177.[Free Full Text]
    45. 45
  45. Russel, N. J. 2002. Bacterial membranes: the effects of chill storage and food processing: an overview. Int. J. Food Microbiol. 79:27-34.[CrossRef][Medline]
    46. 46
  46. Seeliger, H. P. R., and D. Jones. 1984. Listeria, p. 1235-1245. In Bergey's manual of systematic microbiology, vol. 2. Williams & Wilkins, Baltimore, MD.
    47. 47
  47. Snyder, F., and N. Stephens. 1959. A simplified spectrophotometric determination of ester group in lipids. Biochim. Biophys. Acta 34:244-245.[Medline]
    48. 48
  48. Sparling, M. L., R. Zidovetzki, L. Muller, and S. L. Chan. 1989. Analysis of membrane lipids by 500MHz 1H NMR. Anal. Biochem. 178:67-76.[CrossRef][Medline]
    49. 49
  49. Vadyvaloo, V., J. W. Hastings, M. J. van der Merwe, and M. Rautenbach. 2002. Membranes of class IIa bacteriocin-resistant Listeria monocytogenes cells contain increased levels of desaturated and short-acyl-chain phosphatidylglycerols. Appl. Environ. Microbiol. 68:5223-5230.[Abstract/Free Full Text]
    50. 50
  50. Vadyvaloo, V., S. Arous, A. Gravesen, Y. Héchard, R. Chauhan-Haubrock, J. W. Hastings, and M. Rautenbach. 2004. Cell-surface alterations in class IIa bacteriocin-resistant Listeria monocytogenes strains. Microbiology 150:3025-3033.[Abstract/Free Full Text]
    51. 51
  51. Vance, D. E., and C. C. Sweely. 1967. Quantitative determination of neutral glycosyl ceramides in human blood. J. Lipid Res. 8:621-630.[Abstract]
    52. 52
  52. Verheul, A., N. J. Russell, V. T. Hof, F. M. Rombouts, and T. Abee. 1997. Modifications of membrane composition in nisin resistant monocytogenes Scott A. Appl. Environ. Microbiol. 63:3451-3457.[Abstract]
    53. 53
  53. Walker, S., P. Archer, and J. Banks. 1990. Growth of Listeria monocytogenes at refrigeration temperatures. J. Appl. Bacteriol. 68:157-162.[Medline]
    54. 54
  54. Wells, M. A., and J. C. Dittmer. 1966. A microanalytical technique for the quantitative determination of twenty-four classes of brain lipids. Biochemistry 5:3405-3418.[CrossRef][Medline]
    55. 55
  55. Were, L. M., B. Barry, P. M. Davidson, and J. Weiss. 2004. Encapsulation of nisin and lysozyme in liposomes enhances efficacy against Listeria monocytogenes. J. Food Prot. 67:922-927.[Medline]
    56. 56
  56. Winkowski, K., R. P. Ludescher, and T. J. Montville. 1996. Physicochemical characterization of the nisin-membrane interaction with liposomes derived from Listeria monocytogenes. Appl. Environ. Microbiol. 62:323-327.[Abstract]
    57. 57
  57. Zhu, K., X. Ding, M. Julotok, and B. J. Wilkinson. 2005. Exogenous isoleucine and fatty acid shortening ensure the high content of anteiso-C15:0 fatty acid required for low-temperature growth of Listeria monocytogenes. Appl. Environ. Microbiol. 71:8002-8007.[Abstract/Free Full Text]

Applied and Environmental Microbiology, July 2008, p. 4543-4549, Vol. 74, No. 14
0099-2240/08/$08.00+0     doi:10.1128/AEM.02041-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.




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