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. 1997 Oct;63(10):3887–3894. doi: 10.1128/aem.63.10.3887-3894.1997

Critical role of anteiso-C15:0 fatty acid in the growth of Listeria monocytogenes at low temperatures.

B A Annous 1, L A Becker 1, D O Bayles 1, D P Labeda 1, B J Wilkinson 1
PMCID: PMC168698  PMID: 9327552

Abstract

Listeria monocytogenes is a food-borne pathogen capable of growth at refrigeration temperatures. Membrane lipid fatty acids are major determinants of a sufficiently fluid membrane state to allow growth at low temperatures. L. monocytogenes was characterized by a fatty acid profile dominated to an unusual extent (> 95%) by branched-chain fatty acids, with the major fatty acids being anteiso-C15:0, anteiso-C17:0, and iso-C15:0 in cultures grown in complex or defined media at 37 degrees C. Determination of the fatty acid composition of L. monocytogenes 10403S and SLCC 53 grown over the temperature range 45 to 5 degrees C revealed two modes of adaptation of fatty acid composition to lower growth temperatures: (i) shortening of fatty acid chain length and (ii) alteration of branching from iso to anteiso. Two transposon Tn917-induced cold-sensitive mutants incapable of growth at low temperatures had dramatically altered fatty acid compositions with low levels of i-C15:0, a-C15:0, and a-C17:0 and high levels of i-C14:0, C14:0, i-C16:0, and C16:0. The levels of a-C15:0 and a-C17:0 and the ability to grow at low temperatures were restored by supplementing media with 2-methylbutyric acid, presumably because it acted as a precursor of methylbutyryl coenzyme A, the primer for synthesis of anteiso odd-numbered fatty acids. When mid-exponential-phase 10403S cells grown at 37 degrees C were temperature down-shocked to 5 degrees C they were able, for the most part, to reinitiate growth before the membrane fatty acid composition had reset to a composition more typical for low-temperature growth. No obvious evidence was found for a role for fatty acid unsaturation in adaptation of L. monocytogenes to cold temperature. The switch to a fatty acid profile dominated by a-C15:0 at low temperatures and the association of cold sensitivity with deficiency of a-C15:0 focus attention on the critical role of this fatty acid in growth of L. monocytogenes in the cold, presumably through its physical properties and their effects, in maintaining a fluid, liquid-crystalline state of the membrane lipids.

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Selected References

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  1. Amezaga M. R., Davidson I., McLaggan D., Verheul A., Abee T., Booth I. R. The role of peptide metabolism in the growth of Listeria monocytogenes ATCC 23074 at high osmolarity. Microbiology. 1995 Jan;141(Pt 1):41–49. doi: 10.1099/00221287-141-1-41. [DOI] [PubMed] [Google Scholar]
  2. Bayles D. O., Annous B. A., Wilkinson B. J. Cold stress proteins induced in Listeria monocytogenes in response to temperature downshock and growth at low temperatures. Appl Environ Microbiol. 1996 Mar;62(3):1116–1119. doi: 10.1128/aem.62.3.1116-1119.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Camilli A., Portnoy A., Youngman P. Insertional mutagenesis of Listeria monocytogenes with a novel Tn917 derivative that allows direct cloning of DNA flanking transposon insertions. J Bacteriol. 1990 Jul;172(7):3738–3744. doi: 10.1128/jb.172.7.3738-3744.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Denoya C. D., Fedechko R. W., Hafner E. W., McArthur H. A., Morgenstern M. R., Skinner D. D., Stutzman-Engwall K., Wax R. G., Wernau W. C. A second branched-chain alpha-keto acid dehydrogenase gene cluster (bkdFGH) from Streptomyces avermitilis: its relationship to avermectin biosynthesis and the construction of a bkdF mutant suitable for the production of novel antiparasitic avermectins. J Bacteriol. 1995 Jun;177(12):3504–3511. doi: 10.1128/jb.177.12.3504-3511.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Downard J., Toal D. Branched-chain fatty acids: the case for a novel form of cell-cell signalling during Myxococcus xanthus development. Mol Microbiol. 1995 Apr;16(2):171–175. doi: 10.1111/j.1365-2958.1995.tb02290.x. [DOI] [PubMed] [Google Scholar]
  6. Fulco A. J. Fatty acid metabolism in bacteria. Prog Lipid Res. 1983;22(2):133–160. doi: 10.1016/0163-7827(83)90005-x. [DOI] [PubMed] [Google Scholar]
  7. Haest C. W., Verkleij A. J., De Gier J., Scheek R., Ververgaert P. H., Van Deenen L. L. The effect of lipid phase transitions on the architecture of bacterial membranes. Biochim Biophys Acta. 1974 Jul 12;356(1):17–26. doi: 10.1016/0005-2736(74)90290-9. [DOI] [PubMed] [Google Scholar]
  8. Jackson M. B., Cronan J. E., Jr An estimate of the minimum amount of fluid lipid required for the growth of Escherichia coli. Biochim Biophys Acta. 1978 Oct 4;512(3):472–479. doi: 10.1016/0005-2736(78)90157-8. [DOI] [PubMed] [Google Scholar]
  9. Julák J., Ryska M., Koruna I., Mencíková E. Cellular fatty acids and fatty aldehydes of Listeria and Erysipelothrix. Zentralbl Bakteriol. 1989 Dec;272(2):171–180. doi: 10.1016/s0934-8840(89)80003-9. [DOI] [PubMed] [Google Scholar]
  10. Kaneda T. Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev. 1991 Jun;55(2):288–302. doi: 10.1128/mr.55.2.288-302.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ko R., Smith L. T., Smith G. M. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J Bacteriol. 1994 Jan;176(2):426–431. doi: 10.1128/jb.176.2.426-431.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Legendre S., Letellier L., Shechter E. Influence of lipids with branched-chain fatty acids on the physical, morphological and functional properties of Escherichia coli cytoplasmic membrane. Biochim Biophys Acta. 1980 Nov 18;602(3):491–505. doi: 10.1016/0005-2736(80)90328-4. [DOI] [PubMed] [Google Scholar]
  13. Leimeister-Wächter M., Haffner C., Domann E., Goebel W., Chakraborty T. Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of listeria monocytogenes. Proc Natl Acad Sci U S A. 1990 Nov;87(21):8336–8340. doi: 10.1073/pnas.87.21.8336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mastronicolis S. K., German J. B., Smith G. M. Diversity of the polar lipids of the food-borne pathogen Listeria monocytogenes. Lipids. 1996 Jun;31(6):635–640. doi: 10.1007/BF02523834. [DOI] [PubMed] [Google Scholar]
  15. Pine L., Malcolm G. B., Brooks J. B., Daneshvar M. I. Physiological studies on the growth and utilization of sugars by Listeria species. Can J Microbiol. 1989 Feb;35(2):245–254. doi: 10.1139/m89-037. [DOI] [PubMed] [Google Scholar]
  16. Püttmann M., Ade N., Hof H. Dependence of fatty acid composition of Listeria spp. on growth temperature. Res Microbiol. 1993 May;144(4):279–283. doi: 10.1016/0923-2508(93)90012-q. [DOI] [PubMed] [Google Scholar]
  17. Raines L. J., Moss C. W., Farshtchi D., Pittman B. Fatty acids of Listeria monocytogenes. J Bacteriol. 1968 Dec;96(6):2175–2177. doi: 10.1128/jb.96.6.2175-2177.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Salmond G. P., Bycroft B. W., Stewart G. S., Williams P. The bacterial 'enigma': cracking the code of cell-cell communication. Mol Microbiol. 1995 May;16(4):615–624. doi: 10.1111/j.1365-2958.1995.tb02424.x. [DOI] [PubMed] [Google Scholar]
  19. Stucky K., Hagting A., Klein J. R., Matern H., Henrich B., Konings W. N., Plapp R. Cloning and characterization of brnQ, a gene encoding a low-affinity, branched-chain amino acid carrier in Lactobacillus delbrückii subsp. lactis DSM7290. Mol Gen Genet. 1995 Dec 20;249(6):682–690. doi: 10.1007/BF00418038. [DOI] [PubMed] [Google Scholar]
  20. Suutari M., Laakso S. Microbial fatty acids and thermal adaptation. Crit Rev Microbiol. 1994;20(4):285–328. doi: 10.3109/10408419409113560. [DOI] [PubMed] [Google Scholar]
  21. Suutari M., Laakso S. Unsaturated and branched chain-fatty acids in temperature adaptation of Bacillus subtilis and Bacillus megaterium. Biochim Biophys Acta. 1992 Jun 22;1126(2):119–124. doi: 10.1016/0005-2760(92)90281-y. [DOI] [PubMed] [Google Scholar]
  22. Walker S. J., Archer P., Banks J. G. Growth of Listeria monocytogenes at refrigeration temperatures. J Appl Bacteriol. 1990 Feb;68(2):157–162. doi: 10.1111/j.1365-2672.1990.tb02561.x. [DOI] [PubMed] [Google Scholar]
  23. Wallace K. K., Zhao B., McArthur H. A., Reynolds K. A. In vivo analysis of straight-chain and branched-chain fatty acid biosynthesis in three actinomycetes. FEMS Microbiol Lett. 1995 Sep 1;131(2):227–234. doi: 10.1111/j.1574-6968.1995.tb07781.x. [DOI] [PubMed] [Google Scholar]
  24. Willecke K., Pardee A. B. Fatty acid-requiring mutant of bacillus subtilis defective in branched chain alpha-keto acid dehydrogenase. J Biol Chem. 1971 Sep 10;246(17):5264–5272. [PubMed] [Google Scholar]

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