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BioMed Research International
Volume 2014, Article ID 471317, 8 pages
http://dx.doi.org/10.1155/2014/471317
Research Article

Specific Growth Rate Determines the Sensitivity of Escherichia coli to Lactic Acid Stress: Implications for Predictive Microbiology

1Division of Risk and Benefit Assessment, National Food Agency, 75126 Uppsala, Sweden
2Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, 750 07 Uppsala, Sweden
3Department of Microbiology, Swedish University of Agricultural Sciences, 750 07 Uppsala, Sweden
4Department of Forest Products, Swedish University of Agricultural Sciences, 750 07 Uppsala, Sweden

Received 24 April 2014; Accepted 18 June 2014; Published 8 July 2014

Academic Editor: Antonio Valero

Copyright © 2014 Roland Lindqvist and Gunilla Barmark. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. C. Erickson and M. P. Doyle, “Food as a vehicle for transmission of Shiga toxin-producing Escherichia coli,” Journal of Food Protection, vol. 70, no. 10, pp. 2426–2449, 2007. View at Google Scholar · View at Scopus
  2. K. W. Arnold and C. W. Kaspar, “Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7,” Applied and Environmental Microbiology, vol. 61, no. 5, pp. 2037–2039, 1995. View at Google Scholar · View at Scopus
  3. L. L. Duffy, F. H. Grau, and P. B. Vanderlinde, “Acid resistance of enterohaemorrhagic and generic Escherichia coli associated with foodborne disease and meat,” International Journal of Food Microbiology, vol. 60, no. 1, pp. 83–89, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Lindqvist and M. Lindblad, “Time to growth and inactivation of three STEC outbreak strains under conditions relevant for fermented sausages,” International Journal of Food Microbiology, vol. 145, no. 1, pp. 49–56, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. J. W. Foster, “Escherichia coli acid resistance: Tales of an amateur acidophile,” Nature Reviews Microbiology, vol. 2, no. 11, pp. 898–907, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. M. M. Benjamin and A. R. Datta, “Acid tolerance of enterohemorrhagic Escherichia coli,” Applied and Environmental Microbiology, vol. 61, no. 4, pp. 1669–1672, 1995. View at Google Scholar · View at Scopus
  7. R. L. Buchanan and S. G. Edelson, “Culturing enterohemorrhagic Escherichia coli in the presence and absence of glucose as a simple means of evaluating the acid tolerance of stationary—phase cells,” Applied and Environmental Microbiology, vol. 62, no. 11, pp. 4009–4013, 1996. View at Google Scholar · View at Scopus
  8. J. Lin, M. P. Smith, K. C. Chapin, H. S. Baik, G. N. Bennett, and J. W. Foster, “Mechanisms of acid resistance in enterohemorrhagic Escherichia coli,” Applied and Environmental Microbiology, vol. 62, no. 9, pp. 3094–3100, 1996. View at Google Scholar · View at Scopus
  9. R. L. Buchanan and S. G. Edelson, “pH-Dependent stationary-phase acid resistance response of enterohemorrhagic Escherichia coli in the presence of various acidulants,” Journal of Food Protection, vol. 62, no. 3, pp. 211–218, 1999. View at Google Scholar · View at Scopus
  10. Y. Deng, J. Ryu, and L. Beuchat, “Tolerance of acid-adapted and non-adapted Escherichia coli O157:H7 cells to reduced pH as affected by type of acidulant,” Journal of Applied Microbiology, vol. 86, no. 2, pp. 203–210, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. O. J. McQuestin, T. A. McMeekin, and T. Ross, “Effect of suspension media on nonthermal inactivation of Escherichia coli,” Letters in Applied Microbiology, vol. 43, no. 5, pp. 523–527, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. V. Seputiene, A. Daugelavicius, K. Suziedelis, and E. Suziedeliene, “Acid response of exponentially growing Escherichia coli K-12,” Microbiology Research, vol. 161, no. 1, pp. 65–74, 2006. View at Publisher · View at Google Scholar
  13. K. Yokoigawa, A. Takikawa, Y. Okubo, and S. Umesako, “Acid tolerance and gad mRNA levels of Escherichia coli O157:H7 grown in foods,” International Journal of Food Microbiology, vol. 82, no. 3, pp. 203–211, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Hengge-Aronis, “Recent insights into the general stress response regulatory network in Escherichia coli,” Journal of Molecular Microbiology and Biotechnology, vol. 4, no. 3, pp. 341–346, 2002. View at Google Scholar · View at Scopus
  15. J. Ihssen and T. Egli, “Specific growth rate and not cell density controls the general stress response in Escherichia coli,” Microbiology, vol. 150, no. 6, pp. 1637–1648, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Hirakawa, M. Hayashi-Nishino, A. Yamaguchi, and K. Nishino, “Indole enhances acid resistance in Escherichia coli,” Microbial Pathogenesis, vol. 49, no. 3, pp. 90–94, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. S. J. Pirt, “Introductory lecture. Prospects and problems in continuous flow culture of micro-organisms,” Journal of Applied Chemistry and Biotechnology, vol. 22, no. 1, pp. 55–64, 1972. View at Google Scholar
  18. M. Berney, H. Weilenmann, J. Ihssen, C. Bassin, and T. Egli, “Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection,” Applied and Environmental Microbiology, vol. 72, no. 4, pp. 2586–2593, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Lindqvist and M. Lindblad, “Inactivation of Escherichia coli, Listeria monocytogenes and Yersinia enterocolitica in fermented sausages during maturation/storage,” International Journal of Food Microbiology, vol. 129, no. 1, pp. 59–67, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Nanchen, A. Schicker, and U. Sauer, “Nonlinear dependency of intracellular fluxes on growth rate in miniaturized continuous cultures of Escherichia coli,” Applied and Environmental Microbiology, vol. 72, no. 2, pp. 1164–1172, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. A. H. Geeraerd, V. P. Valdramidis, and J. F. van Impe, “GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves,” International Journal of Food Microbiology, vol. 102, no. 1, pp. 95–105, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. T. M. Bergholz, L. M. Wick, W. Qi, J. T. Riordan, L. M. Ouellette, and T. S. Whittam, “Global transcriptional response of Escherichia coli O157:H7 to growth transitions in glucose minimal medium,” BMC Microbiology, vol. 7, article 97, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Ross, D. Zhang, and O. J. McQuestin, “Temperature governs the inactivation rate of vegetative bacteria under growth-preventing conditions,” International Journal of Food Microbiology, vol. 128, no. 1, pp. 129–135, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. O. J. McQuestin, C. T. Shadbolt, and T. Ross, “Quantification of the relative effects of temperature, pH, and water activity on inactivation of Escherichia coli in fermented meat by meta-analysis,” Applied and Environmental Microbiology, vol. 75, no. 22, pp. 6963–6972, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. J. J. Semanchek and D. A. Golden, “Influence of growth temperature on inactivation and injury of Escherichia coli O157:H7 by heat, acid, and freezing,” Journal of Food Protection, vol. 61, no. 4, pp. 395–401, 1998. View at Google Scholar · View at Scopus
  26. G. Cebrián, N. Sagarzazu, R. Pagán, S. Condón, and P. Mañas, “Resistance of Escherichia coli grown at different temperatures to various environmental stresses,” Journal of Applied Microbiology, vol. 105, no. 1, pp. 271–278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. N. G. Faith, N. Parniere, T. Larson, T. D. Lorang, C. W. Kaspar, and J. B. Luchansky, “Viability of Escherichia coli O157:H7 in salami following conditioning of batter, fermentation and drying of sticks, and storage of slices,” Journal of Food Protection, vol. 61, no. 4, pp. 377–382, 1998. View at Google Scholar · View at Scopus