Role of branched-chain fatty acids in pH stress tolerance in Listeria monocytogenes

E S Giotis, DA McDowell, I S Blair, B J Wilkinson

    Research output: Contribution to journalArticle

    77 Citations (Scopus)

    Abstract

    In alkaline conditions, Listeria monocytogenes cells develop higher proportions of branched-chain fatty acids (FAs), including more anteiso forms. In acid conditions, the opposite occurs. Reduced growth of pH-sensitive mutants at adverse pH (5.0/9.0) was alleviated by the addition of 2 -methylbutyrate (an anteiso-FA precursor), suggesting that anteiso-FAs are important in adaptation to adverse pH. The balance between anteiso- and iso-FAs may be more important than changes in the amounts and/or degrees of saturation of FAs in pH adaptation.
    LanguageEnglish
    Pages997-1001
    JournalApplied and Environmental Microbiology
    Volume73
    Issue number3
    DOIs
    Publication statusPublished - 2007

    Fingerprint

    branched chain fatty acids
    Listeria monocytogenes
    stress tolerance
    Fatty Acids
    fatty acid
    tolerance
    fatty acids
    mutants
    saturation
    acids
    Acids
    acid
    Growth
    cells

    Keywords

    • membrane-lipid-composition
    • streptococcus-mutans
    • bacillus-subtilis
    • escherichia-coli
    • enhance survival
    • low-temperatures
    • growth
    • adaptation
    • resistance
    • biosynthesis

    Cite this

    Giotis, E S ; McDowell, DA ; Blair, I S ; Wilkinson, B J. / Role of branched-chain fatty acids in pH stress tolerance in Listeria monocytogenes. In: Applied and Environmental Microbiology. 2007 ; Vol. 73, No. 3. pp. 997-1001.
    @article{d3f991f7a15146e598efe4bd472fd1fe,
    title = "Role of branched-chain fatty acids in pH stress tolerance in Listeria monocytogenes",
    abstract = "In alkaline conditions, Listeria monocytogenes cells develop higher proportions of branched-chain fatty acids (FAs), including more anteiso forms. In acid conditions, the opposite occurs. Reduced growth of pH-sensitive mutants at adverse pH (5.0/9.0) was alleviated by the addition of 2 -methylbutyrate (an anteiso-FA precursor), suggesting that anteiso-FAs are important in adaptation to adverse pH. The balance between anteiso- and iso-FAs may be more important than changes in the amounts and/or degrees of saturation of FAs in pH adaptation.",
    keywords = "membrane-lipid-composition, streptococcus-mutans, bacillus-subtilis, escherichia-coli, enhance survival, low-temperatures, growth, adaptation, resistance, biosynthesis",
    author = "Giotis, {E S} and DA McDowell and Blair, {I S} and Wilkinson, {B J}",
    note = "Reference text: 1. 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. 63:3887–3894. 2. Bayles, D. O., and B. J. Wilkinson. 2000. Osmoprotectants and cryoprotectants for Listeria monocytogenes. Lett. Appl. Microbiol. 30:23–27. 3. Becker, L. A., S. N. Evans, R. W. Hutkins, and A. K. Benson. 2000. Role of B in adaptation of Listeria monocytogenes to growth at low temperature. J. Bacteriol. 182:7083–7087. 4. Bower, C. K., and M. A. Daeschel. 1999. Resistance responses of microorganisms in food environments. Int. J. Food Microbiol. 50:33–44. 5. Brown, J. L., T. Ross, T. A. McMeekin, and P. D. Nichols. 1997. Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int. J. Food Microbiol. 37:163–173. 6. Butler, T., R. W. Frenck, R. B. Johnson, and R. Khakhria. 2001. In vitro effects of azithromycin on Salmonella typhi: early inhibition by concentrations less than the MIC and reduction of MIC by alkaline pH and small inocula. J. Antimicrob. Chemother. 47:455–458. 7. Chihib, N. E., M. Ribeiro da Silva, G. Delattre, M. Laroche, and M. Federighi. 2003. Different cellular fatty acid pattern behaviours of two strains of Listeria monocytogenes Scott A and CNL 895807 under different temperature and salinity conditions. FEMS Microbiol. Lett. 218:155– 160. 8. Choi, K. H., R. J. Heath, and C. O. Rock. 2000. Beta-ketoacyl-acyl carrier protein synthase III (FabH) is a determining factor in branched-chain fatty acid biosynthesis. J. Bacteriol. 182:365–370. 9. Clejan, S., T. A. Krulwich, K. R. Mondrus, and D. Setoyoung. 1986. Membrane lipid composition of obligately and facultatively alkalophilic strains of Bacillus spp. J. Bacteriol. 168:334–340. 10. Cronan, J. E. 2003. Bacterial membrane lipids: where do we stand? Annul Rev. Microbiol. 57:203–224. 11. Deinhard, G., J. Saar, W. Krischke, and K. Poralla. 1987. Bacillus cycloheptanicus sp-Nov, a new thermoacidophile containing omega-cycloheptane fatty acids. Syst. Appl. Microbiol. 10:68–73. 12. De Mendoza, D., G. E. Schujman, and P. S. Aguilar. 2002. Biosynthesis and function of membrane lipids, p. 43–55. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. American Society for Microbiology, Washington, DC. 13. Dubois-Brissonnet, F., C. Malgrange, L. Guerin-Mechin, B. Heyd, and J. Y. Leveau. 2001. Changes in fatty acid composition of Pseudomonas aeruginosa ATCC 15442 induced by growth conditions: consequences of resistance to quaternary ammonium compounds. Microbios 106:97–110. 14. Edgcomb, M. R., S. Sirimanne, B. J. Wilkinson, P. Drouin, and R. Morse 2000. Electron paramagnetic resonance studies of the membrane fluidity of the foodborne pathogenic psychrotroph Listeria monocytogenes. Biochim. Biophys. Acta 1463:31–42. 15. Farber, J. M., and P. I. Peterkin. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiol. Rev. 55:476–511. 16. Fozo, E. M., and R. G. Quivey, Jr. 2004. Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl. Environ. Microbiol. 70:929–936. 17. Fozo, E. M., J. K. Kajfasz, and R. G. Quivey. 2004. Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol. Lett. 238:291– 295. 18. Fozo, E. M., and R. G. Quivey, Jr. 2004. The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J. Bacteriol. 186:4152–4158. 19. Gahan, C. G. M., B. O’Driscoll, and C. Hill. 1996. Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Appl. Environ. Microbiol. 62:3128–3132. 20. Julak, J., M. Ryska, I. Koruna, and E. Mencikova. 1989. Cellular fatty acids and fatty aldehydes of Listeria and Erysipelothrix. Zentbl. Bakteriol. Int. J. Med. Microbiol. 272:171–180. 21. Jydegaard-Axelsen, A.-M., P. E. H{\o}iby, K. Holmstr{\o}m, N. Russell, and S. Kn{\o}chel. 2004. CO2- and anaerobiosis-induced changes in physiology and gene expression of different Listeria monocytogenes strains. Appl. Environ. Microbiol. 70:4111–4117. 22. Kaneda, T. 1977. Fatty acids of genus Bacillus: an example of branched-chain preference. Bacteriol. Rev. 41:391–418. 23. Kaneda, T. 1991. Iso-fatty and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55:288–302. 24. Kim, B. H., S. Kim, H. G. Kim, J. Lee, I. S. Lee, and Y. K. Park. 2005. The formation of cyclopropane fatty acids in Salmonella enterica serovar typhimurium. Microbiology 151:209–218. 25. Klein, W., M. H. W. Weber, and M. A. Marahiel. 1999. Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J. Bacteriol. 181: 5341–5349. 26. Li, J., M. L. Chikindas, R. D. Ludescher, and T. J. Montville. 2002. Temperature and surfactant-induced membrane modifications that alter Listeria monocytogenes nisin sensitivity by different mechanisms. Appl. Environ. Microbiol. 68:5904–5910. 27. Lou, Y. Q., and A. E. Yousef. 1997. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Appl. Environ. Microbiol. 63:1252–1255. 28. Lu, Y. J., Y. M. Zhang, and C. O. Rock. 2004. Product diversity and regulation of type II fatty acid synthases. Biochem. Cell Biol. 82:145–155. 29. 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. 30. Mendonca, A. F., T. L. Amoroso, and S. J. Knabel. 1994. Destruction of gram-negative food-borne pathogens by high pH involves disruption of the cytoplasmic membrane. Appl. Environ. Microbiol. 60:4009–4014. 31. Neumann, G., N. Kabelitz, and H. J. Heipieper. 2003. The regulation of the cis-trans isomerase of unsaturated fatty acids in Pseudomonas putida: correlation between cti activity and K uptake systems. Eur. J. Lipid Sci. Technol. 105:585–589. 32. Nichols, D. S., K. A. Presser, J. Olley, T. Ross, and T. A. McMeekin. 2002. Variation of branched-chain fatty acids marks the normal physiological range for growth in Listeria monocytogenes. Appl. Environ. Microbiol. 68: 2809–2813. 33. Nickerson, K. W., and L. A. Bulla. 1980. Incorporation of specific fatty acid precursors during spore germination and outgrowth in Bacillus thuringiensis. Appl. Environ. Microbiol. 40:166–168. 34. Nielsen, L. E., D. R. Kadavy, S. Rajagopal, R. Drijber, and K. W. Nickerson. 2005. Survey of extreme solvent tolerance in gram-positive cocci: membrane fatty acid changes in Staphylococcus haemolyticus grown in toluene. Appl. Environ. Microbiol. 71:5171–5176. 35. O’Driscoll, B., C. G. M. Gahan, and C. Hill. 1996. Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl. Environ. Microbiol. 62:1693– 1698. 36. Oku, H., K. Fujita, T. Nomoto, K. Suzuki, H. Iwasaki, and I. Chinen. 1998. NADH-dependent inhibition of branched-chain fatty acid synthesis in Bacillus subtilis. Biosci. Biotechnol. Biochem. 62:622–627. 37. Oku, H., and T. Kaneda. 1988. Biosynthesis of branched-chain fatty acids in Bacillus subtilis. a decarboxylase is essential for branched-chain fatty acid synthetase. J. Biol. Chem. 263:18386–18396. 38. Pearson, L. J., and E. H. Marth. 1990. Listeria monocytogenes—threat to a safe food supply: a review. J. Dairy Sci. 73:912–928. 39. Poralla, K., and W. A. Konig. 1983. The occurrence of omega-cycloheptane fatty acids in a thermo-acidophilic Bacillus. FEMS Microbiol. Lett. 16:303– 306. 40. Russell, N. J. 2002. Bacterial membranes: the effects of chill storage and food processing. An overview. Int. J. Food Microbiol. 79:27–34. 41. Russell, N. J., R. I. Evans, P. F. Steeg, J. Hellemons, A. Verheul, and T. Abee. 1995. Membranes as a target for stress adaptation. Int. J. Food Microbiol. 28:255–261. 42. Sharma, M., P. J. Taormina, and L. R. Beuchat. 2003. Habituation of foodborne pathogens exposed to extreme pH conditions: genetic basis and implications in foods and food processing environments. Food Sci. Technol. Res. 9:115–127. 43. Taormina, P. J., and L. R. Beuchat. 2002. Survival and growth of alkali stressed Listeria monocytogenes on beef frankfurters and thermotolerance in frankfurter exudates. J. Food Prot. 65:291–298. 44. Taormina, P. J., and L. R. Beuchat. 2001. Survival and heat resistance of Listeria monocytogenes after exposure to alkali and chlorine. Appl. Environ. Microbiol. 67:2555–2563. 45. Taormina, P. J., and L. R. Beuchat. 2002. Survival of Listeria monocytogenes in commercial food-processing equipment cleaning solutions and subsequent sensitivity to sanitizers and heat. J. Appl. Microbiol. 92:71–80. 46. Tienungoon, S., D. A. Ratkowsky, T. A. McMeekin, and T. Ross. 2000. Growth limits of Listeria monocytogenes as a function of temperature, pH, NaCl, and lactic acid. Appl. Environ. Microbiol. 66:4979–4987. 47. Yeo, I. H., S. K. Han, J. H. Yu, and D. H. Bai. 1998. Isolation of novel alkalophilic Bacillus alcalophilus subsp. YB380 and the characteristics of its yeast cell wall hydrolase. J. Microbiol. Biotechnol. 8:501–508. 48. Yuk, H.-G., and D. L. Marshall. 2004. Adaptation of Escherichia coli O157:H7 to pH alters membrane lipid composition, verotoxin secretion, and resistance to simulated gastric fluid acid. Appl. Environ. Microbiol. 70:3500–3505. 49. Zhu, K., D. O. Bayles, A. M. Xiong, R. K. Jayaswal, and B. J. Wilkinson. 2005. Precursor and temperature modulation of fatty acid composition and growth of Listeria monocytogenes cold-sensitive mutants with transposon interrupted branched-chain alpha-keto acid dehydrogenase. Microbiology 151:615–623. 50. 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.",
    year = "2007",
    doi = "10.1128/AEM.00865-06",
    language = "English",
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    pages = "997--1001",
    journal = "Applied and Environmental Microbiology",
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    publisher = "American Society for Microbiology",
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    }

    Role of branched-chain fatty acids in pH stress tolerance in Listeria monocytogenes. / Giotis, E S; McDowell, DA; Blair, I S; Wilkinson, B J.

    In: Applied and Environmental Microbiology, Vol. 73, No. 3, 2007, p. 997-1001.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Role of branched-chain fatty acids in pH stress tolerance in Listeria monocytogenes

    AU - Giotis, E S

    AU - McDowell, DA

    AU - Blair, I S

    AU - Wilkinson, B J

    N1 - Reference text: 1. 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. 63:3887–3894. 2. Bayles, D. O., and B. J. Wilkinson. 2000. Osmoprotectants and cryoprotectants for Listeria monocytogenes. Lett. Appl. Microbiol. 30:23–27. 3. Becker, L. A., S. N. Evans, R. W. Hutkins, and A. K. Benson. 2000. Role of B in adaptation of Listeria monocytogenes to growth at low temperature. J. Bacteriol. 182:7083–7087. 4. Bower, C. K., and M. A. Daeschel. 1999. Resistance responses of microorganisms in food environments. Int. J. Food Microbiol. 50:33–44. 5. Brown, J. L., T. Ross, T. A. McMeekin, and P. D. Nichols. 1997. Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int. J. Food Microbiol. 37:163–173. 6. Butler, T., R. W. Frenck, R. B. Johnson, and R. Khakhria. 2001. In vitro effects of azithromycin on Salmonella typhi: early inhibition by concentrations less than the MIC and reduction of MIC by alkaline pH and small inocula. J. Antimicrob. Chemother. 47:455–458. 7. Chihib, N. E., M. Ribeiro da Silva, G. Delattre, M. Laroche, and M. Federighi. 2003. Different cellular fatty acid pattern behaviours of two strains of Listeria monocytogenes Scott A and CNL 895807 under different temperature and salinity conditions. FEMS Microbiol. Lett. 218:155– 160. 8. Choi, K. H., R. J. Heath, and C. O. Rock. 2000. Beta-ketoacyl-acyl carrier protein synthase III (FabH) is a determining factor in branched-chain fatty acid biosynthesis. J. Bacteriol. 182:365–370. 9. Clejan, S., T. A. Krulwich, K. R. Mondrus, and D. Setoyoung. 1986. Membrane lipid composition of obligately and facultatively alkalophilic strains of Bacillus spp. J. Bacteriol. 168:334–340. 10. Cronan, J. E. 2003. Bacterial membrane lipids: where do we stand? Annul Rev. Microbiol. 57:203–224. 11. Deinhard, G., J. Saar, W. Krischke, and K. Poralla. 1987. Bacillus cycloheptanicus sp-Nov, a new thermoacidophile containing omega-cycloheptane fatty acids. Syst. Appl. Microbiol. 10:68–73. 12. De Mendoza, D., G. E. Schujman, and P. S. Aguilar. 2002. Biosynthesis and function of membrane lipids, p. 43–55. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. American Society for Microbiology, Washington, DC. 13. Dubois-Brissonnet, F., C. Malgrange, L. Guerin-Mechin, B. Heyd, and J. Y. Leveau. 2001. Changes in fatty acid composition of Pseudomonas aeruginosa ATCC 15442 induced by growth conditions: consequences of resistance to quaternary ammonium compounds. Microbios 106:97–110. 14. Edgcomb, M. R., S. Sirimanne, B. J. Wilkinson, P. Drouin, and R. Morse 2000. Electron paramagnetic resonance studies of the membrane fluidity of the foodborne pathogenic psychrotroph Listeria monocytogenes. Biochim. Biophys. Acta 1463:31–42. 15. Farber, J. M., and P. I. Peterkin. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiol. Rev. 55:476–511. 16. Fozo, E. M., and R. G. Quivey, Jr. 2004. Shifts in the membrane fatty acid profile of Streptococcus mutans enhance survival in acidic environments. Appl. Environ. Microbiol. 70:929–936. 17. Fozo, E. M., J. K. Kajfasz, and R. G. Quivey. 2004. Low pH-induced membrane fatty acid alterations in oral bacteria. FEMS Microbiol. Lett. 238:291– 295. 18. Fozo, E. M., and R. G. Quivey, Jr. 2004. The fabM gene product of Streptococcus mutans is responsible for the synthesis of monounsaturated fatty acids and is necessary for survival at low pH. J. Bacteriol. 186:4152–4158. 19. Gahan, C. G. M., B. O’Driscoll, and C. Hill. 1996. Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Appl. Environ. Microbiol. 62:3128–3132. 20. Julak, J., M. Ryska, I. Koruna, and E. Mencikova. 1989. Cellular fatty acids and fatty aldehydes of Listeria and Erysipelothrix. Zentbl. Bakteriol. Int. J. Med. Microbiol. 272:171–180. 21. Jydegaard-Axelsen, A.-M., P. E. Høiby, K. Holmstrøm, N. Russell, and S. Knøchel. 2004. CO2- and anaerobiosis-induced changes in physiology and gene expression of different Listeria monocytogenes strains. Appl. Environ. Microbiol. 70:4111–4117. 22. Kaneda, T. 1977. Fatty acids of genus Bacillus: an example of branched-chain preference. Bacteriol. Rev. 41:391–418. 23. Kaneda, T. 1991. Iso-fatty and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55:288–302. 24. Kim, B. H., S. Kim, H. G. Kim, J. Lee, I. S. Lee, and Y. K. Park. 2005. The formation of cyclopropane fatty acids in Salmonella enterica serovar typhimurium. Microbiology 151:209–218. 25. Klein, W., M. H. W. Weber, and M. A. Marahiel. 1999. Cold shock response of Bacillus subtilis: isoleucine-dependent switch in the fatty acid branching pattern for membrane adaptation to low temperatures. J. Bacteriol. 181: 5341–5349. 26. Li, J., M. L. Chikindas, R. D. Ludescher, and T. J. Montville. 2002. Temperature and surfactant-induced membrane modifications that alter Listeria monocytogenes nisin sensitivity by different mechanisms. Appl. Environ. Microbiol. 68:5904–5910. 27. Lou, Y. Q., and A. E. Yousef. 1997. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Appl. Environ. Microbiol. 63:1252–1255. 28. Lu, Y. J., Y. M. Zhang, and C. O. Rock. 2004. Product diversity and regulation of type II fatty acid synthases. Biochem. Cell Biol. 82:145–155. 29. 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. 30. Mendonca, A. F., T. L. Amoroso, and S. J. Knabel. 1994. Destruction of gram-negative food-borne pathogens by high pH involves disruption of the cytoplasmic membrane. Appl. Environ. Microbiol. 60:4009–4014. 31. Neumann, G., N. Kabelitz, and H. J. Heipieper. 2003. The regulation of the cis-trans isomerase of unsaturated fatty acids in Pseudomonas putida: correlation between cti activity and K uptake systems. Eur. J. Lipid Sci. Technol. 105:585–589. 32. Nichols, D. S., K. A. Presser, J. Olley, T. Ross, and T. A. McMeekin. 2002. Variation of branched-chain fatty acids marks the normal physiological range for growth in Listeria monocytogenes. Appl. Environ. Microbiol. 68: 2809–2813. 33. Nickerson, K. W., and L. A. Bulla. 1980. Incorporation of specific fatty acid precursors during spore germination and outgrowth in Bacillus thuringiensis. Appl. Environ. Microbiol. 40:166–168. 34. Nielsen, L. E., D. R. Kadavy, S. Rajagopal, R. Drijber, and K. W. Nickerson. 2005. Survey of extreme solvent tolerance in gram-positive cocci: membrane fatty acid changes in Staphylococcus haemolyticus grown in toluene. Appl. Environ. Microbiol. 71:5171–5176. 35. O’Driscoll, B., C. G. M. Gahan, and C. Hill. 1996. Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Appl. Environ. Microbiol. 62:1693– 1698. 36. Oku, H., K. Fujita, T. Nomoto, K. Suzuki, H. Iwasaki, and I. Chinen. 1998. NADH-dependent inhibition of branched-chain fatty acid synthesis in Bacillus subtilis. Biosci. Biotechnol. Biochem. 62:622–627. 37. Oku, H., and T. Kaneda. 1988. Biosynthesis of branched-chain fatty acids in Bacillus subtilis. a decarboxylase is essential for branched-chain fatty acid synthetase. J. Biol. Chem. 263:18386–18396. 38. Pearson, L. J., and E. H. Marth. 1990. Listeria monocytogenes—threat to a safe food supply: a review. J. Dairy Sci. 73:912–928. 39. Poralla, K., and W. A. Konig. 1983. The occurrence of omega-cycloheptane fatty acids in a thermo-acidophilic Bacillus. FEMS Microbiol. Lett. 16:303– 306. 40. Russell, N. J. 2002. Bacterial membranes: the effects of chill storage and food processing. An overview. Int. J. Food Microbiol. 79:27–34. 41. Russell, N. J., R. I. Evans, P. F. Steeg, J. Hellemons, A. Verheul, and T. Abee. 1995. Membranes as a target for stress adaptation. Int. J. Food Microbiol. 28:255–261. 42. Sharma, M., P. J. Taormina, and L. R. Beuchat. 2003. Habituation of foodborne pathogens exposed to extreme pH conditions: genetic basis and implications in foods and food processing environments. Food Sci. Technol. Res. 9:115–127. 43. Taormina, P. J., and L. R. Beuchat. 2002. Survival and growth of alkali stressed Listeria monocytogenes on beef frankfurters and thermotolerance in frankfurter exudates. J. Food Prot. 65:291–298. 44. Taormina, P. J., and L. R. Beuchat. 2001. Survival and heat resistance of Listeria monocytogenes after exposure to alkali and chlorine. Appl. Environ. Microbiol. 67:2555–2563. 45. Taormina, P. J., and L. R. Beuchat. 2002. Survival of Listeria monocytogenes in commercial food-processing equipment cleaning solutions and subsequent sensitivity to sanitizers and heat. J. Appl. Microbiol. 92:71–80. 46. Tienungoon, S., D. A. Ratkowsky, T. A. McMeekin, and T. Ross. 2000. Growth limits of Listeria monocytogenes as a function of temperature, pH, NaCl, and lactic acid. Appl. Environ. Microbiol. 66:4979–4987. 47. Yeo, I. H., S. K. Han, J. H. Yu, and D. H. Bai. 1998. Isolation of novel alkalophilic Bacillus alcalophilus subsp. YB380 and the characteristics of its yeast cell wall hydrolase. J. Microbiol. Biotechnol. 8:501–508. 48. Yuk, H.-G., and D. L. Marshall. 2004. Adaptation of Escherichia coli O157:H7 to pH alters membrane lipid composition, verotoxin secretion, and resistance to simulated gastric fluid acid. Appl. Environ. Microbiol. 70:3500–3505. 49. Zhu, K., D. O. Bayles, A. M. Xiong, R. K. Jayaswal, and B. J. Wilkinson. 2005. Precursor and temperature modulation of fatty acid composition and growth of Listeria monocytogenes cold-sensitive mutants with transposon interrupted branched-chain alpha-keto acid dehydrogenase. Microbiology 151:615–623. 50. 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.

    PY - 2007

    Y1 - 2007

    N2 - In alkaline conditions, Listeria monocytogenes cells develop higher proportions of branched-chain fatty acids (FAs), including more anteiso forms. In acid conditions, the opposite occurs. Reduced growth of pH-sensitive mutants at adverse pH (5.0/9.0) was alleviated by the addition of 2 -methylbutyrate (an anteiso-FA precursor), suggesting that anteiso-FAs are important in adaptation to adverse pH. The balance between anteiso- and iso-FAs may be more important than changes in the amounts and/or degrees of saturation of FAs in pH adaptation.

    AB - In alkaline conditions, Listeria monocytogenes cells develop higher proportions of branched-chain fatty acids (FAs), including more anteiso forms. In acid conditions, the opposite occurs. Reduced growth of pH-sensitive mutants at adverse pH (5.0/9.0) was alleviated by the addition of 2 -methylbutyrate (an anteiso-FA precursor), suggesting that anteiso-FAs are important in adaptation to adverse pH. The balance between anteiso- and iso-FAs may be more important than changes in the amounts and/or degrees of saturation of FAs in pH adaptation.

    KW - membrane-lipid-composition

    KW - streptococcus-mutans

    KW - bacillus-subtilis

    KW - escherichia-coli

    KW - enhance survival

    KW - low-temperatures

    KW - growth

    KW - adaptation

    KW - resistance

    KW - biosynthesis

    U2 - 10.1128/AEM.00865-06

    DO - 10.1128/AEM.00865-06

    M3 - Article

    VL - 73

    SP - 997

    EP - 1001

    JO - Applied and Environmental Microbiology

    T2 - Applied and Environmental Microbiology

    JF - Applied and Environmental Microbiology

    SN - 0099-2240

    IS - 3

    ER -