Acetic acid induces pH-independent cellular energy depletion in salmonella enterica

Foodborne Pathogens and Disease

Volumn 12, Issue 3, 2015, Pages 183-189

  Tan, Sin Mei ^a   Lee, Sui Mae ^a   Dykes, Gary A ^a,b  

^a MONASH UNIVERSITY MALAYSIA   (Malaysia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ADENINE NUCLEOTIDE TRANSLOCASE; LACTIC ACID; SORBIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DISINFECTANT AGENT;

ACIDITY; ARTICLE; ATPASE ACTIVITY ASSAY; BACTERIAL CELL WALL; BACTERIAL STRAIN; CELL ENERGY; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; MEMBRANE DAMAGE; NONHUMAN; NUCLEIC ACID ANALYSIS; PH; PKA; PRIORITY JOURNAL; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SCANNING ELECTRON MICROSCOPY; CHEMISTRY; DRUG EFFECTS; SALMONELLA ENTERICA; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA;

ACETIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DISINFECTANTS; HYDROGEN-ION CONCENTRATION; MICROSCOPY, ELECTRON, SCANNING; SALMONELLA ENTERICA;

EID: 84924692699     PISSN: 15353141     EISSN: 15567125     Source Type: Journal    
DOI: 10.1089/fpd.2014.1853     Document Type: Article

References (39)

1. Alakomi HL, Skytta E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM. Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 2000;66:2001-2005
2. Anderson RJ, Groundwater PW, Todd A, Worsley AJ. Antibacterial Agents: Chemistry, Mode of Action, Mechanisms of Resistance and Clinical Applications. Chichester, UK: John Wiley & Sons Ltd., 2012
3. Aslim B, Yuksekdag ZN, Sarikaya E, Belyati Y. Determination of the bacteriocin-like substances produced by some lactic acid bacteria isolated from Turkish dairy products. Swiss Soc Food Sci Technol 2005;38:691-694
4. Bereksi N, Gavini F, Bénézech T, Faille C. Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. J Appl Microbiol 2002;92:556-565
5. Bracey D, Holyoak CD, Coote PJ. Comparison of the inhibitory effect of sorbic acid and amphotericin B on Saccharomyces cerevisiae: Is growth inhibition dependent on reduced intracellular pH?. J Appl Microbiol 1998;85:1056-1066
6. Brul S, Coote P. Preservative agents in foods: Mode of action and microbial resistance mechanisms. Int J Food Microbiol 1999;50:1-17
7. Cherrington CA, Hinton M, Chopra I. Effect of short-chain organic acids on macromolecular synthesis in Escherichia coli. J Appl Bacteriol 1990;68:69-74
8. Cherrington CA, Hinton M, Pearson GR, Chopra I. Short-chain organic acids at pH 5.0 kill Escherichia coli and Salmonella spp. without causing membrane perturbation. J Appl Bacteriol 1991;70:161-165
9. DAoust J,Maurer JJ. Salmonella species. In: Food Microbiology: Fundamentals and Frontiers.Doyle MP,Beuchat LR,Montvilles TJ (eds.). Washington, DC: ASM Press, 2007, pp.141-178
10. Davidson PM. Chemical preservatives and natural antimicrobial compounds. In: Food Microbiology: Fundamentals and Frontiers. Doyle MP, Beuchat LR, Montvilles TJ (eds.). Washington, DC: ASM Press, 2001, pp. 593-627
11. den Besten HMW, Mols M, Moezelaar R, Zwietering MH, Abee T. Phenotypic and transcriptomic analysis of mildly and severely salt-stressed Bacillus cereus ATCC 14579 cells. Appl Environ Microbiol 2009;75:4111-4119
12. Dolezalová M, Molatová Z, Buňka F, Březina P, Marounek M. Effect of organic acids on growth of chilled chicken skin microflora. J Food Saf 2010;30:353-365
13. Dykes GA. Physical and metabolic causes of sub-lethal damage in Listeria monocytogenes after long-Term chilled storage at 4C. J Appl Microbiol 1999;87:915-922
14. Eklund T. The antimicrobial effect of dissociated and undissociated sorbic acid at different pH levels. J Appl Bacteriol 1983;54:383-389
15. Eklund T. Inhibition of microbial growth at different pH levels by benzoic and propionic acids and esters of p-hydroxybenzoic acid. Int J Food Microbiol 1985;2:159-167
16. [FDA] Food andDrugAdministration. SelectCommittee on GRAS Substances (SCOGS) Opinion: Acetic Acid. 2013. Available at: http://www.fda.gov/food/ingredientspackaginglabeling/gras/.scogs/ucm255100.htm, accessed July 12, 2014
17. Giotis ES, Blair IS, McDowell DA. Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress. Int J Food Microbiol 2007;120:250-258
18. González-Fandos E, Herrera B, Maya N. Efficacy of citric acid against Listeria monocytogenes attached to poultry skin during refrigerated storage. Int J Food Sci Tech 2009;44: 262-268
19. Helander IM, Mattila-Sandholm T. Fluorometric assessment of gram-negative bacterial permeabilization. J Appl Microbiol 2000;88:213-219
20. Hinton MH, Corry JEL. Poultry Meat Science. Oxon: Cabi Publishing, 1999
21. Jones TH, Gill CO, McMullen LM. Behaviour of log-phase Escherichia coli at temperatures near the minimum for growth. Int J Food Microbiol 2003;88:55-61
22. Jones TH, Vail KM, McMullen LM. Filament formation by foodborne bacteria under sublethal stress. Int J Food Microbiol 2013;165:97-110
23. Jydegaard-Axelsen A, Aaes-Jørgenson A, Koch AG, Jensen JS, Knøchel S. Changes in growth, rRNA content and cell morphology of Listeria monocytogenes induced by CO2 up- And downshift. Int J Food Microbiol 2005;98:145-155
24. Liao CH, Shollenberger LM, Phillips JG. Lethal and sublethal action of acetic acid on Salmonella in vitro and on cut surfaces of apple slices. J Food Sci 2003;68:2793-2798
25. Maiorella B, Blanch HW, Wilke CR. By-product inhibition effects on ethanolic fermentation by Saccharomyces cerevisiae. Biotech Bioeng 1983;25:103-121
26. Mani-López E, García HS, López-Malo A. Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res Int 2012;45:713-721
27. Narendranath NV, Thomas KC, Ingledew WM. Effects of acetic acid and lactic acid on the growth of Saccharomyces cerevisiae in a minimal medium. J Ind Microbiol Biotechnol 2001;26:171-177
28. Nazer AI, Kobilinsky A, Tholozan JL, Dubois-Brisonnet F. Combinations of food antimicrobials at low-levels to inhibit the growth of Salmonella sv. Typhimurium: A synergistic effect?. Food Microbiol 2005;22:391-398
29. Over KF, Hettiarachchy N, Johnson MG, Davis, B. Effect of organic acids and plant extracts on Escherichia coli O157:H7, Listeria monocytogenes and Salmonella Typhimurium in broth culture model and chicken meat systems. J Food Sci 2009;74:515-521
30. Ricke SC. Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poult Sci 2003;82:632-639
31. Roth LA, Keenan D. Acid injury in Escherichia coli. Can J Microbiol 1971;17:1005-1008
32. Russell JB. Another explanation for the toxicity of fermentation acids at low pH: Anion accumulation versus uncoupling. J Appl Bacteriol 1992;73:363-370
33. Salmond CV, Kroll RG, Booth IR. The effect of food preservatives on pH homeostasis in Escherichia coli. J Gen Microbiol 1984;130:2845-2850
34. Smaoui S, Ben-Hlima H, Ben-Salah R, Ghorbel R. Effects of sodium lactate and lactic acid on chemical, microbiological and sensory characteristics of marinated chicken. Afr J Biotechnol 2011;10:11317-11326
35. Stratford M, Anslow PA. Evidence that sorbic acid does not inhibit yeast as a classic weak acid preservatives. Lett Appl Microbiol 1998;27:203-206
36. Sutton NA, Hughes N, Handley PS. A comparison of conventional SEM techniques, low temperature SEM and the wet scanning electron microscope to study the structure of a biofilm of Streptococcus crista CR3. J Appl Bacteriol 1993;76:448-454
37. Tamblyn KC, Conner DE. Bactericidal activity of organic acids against Salmonella Typhimurium attached to broiler chicken skin. J Food Prot 1997;60:629-633
38. Tan SM, Lee SM, Dykes GA. Buffering effect of chicken skin and meat protects Salmonella enterica strains against hydrochloric acid but not organic acid treatment. Food Control 2014;42:329-334
39. Thompson JL, Hinton M. Effect of short-chain fatty acids on the size of enteric bacteria. Lett Appl Microbiol 1996;22: 408-412