Stress Induction and Response, Inactivation, and Recovery of Vegetative Microorganisms by Pulsed Electric Fields

  • Felix Schottroff
  • Anna Krottenthaler
  • Henry Jaeger
Living reference work entry

Abstract

Electroporation phenomena can be distinguished by the reversibility of the membrane permeabilization. This definition, however, takes into account structural aspects only. It does not include the physiological state of the microorganisms, which is another key aspect in order to characterize the vitality of cells. Depending on the strain, matrix, and process intensity, sublethal injury, a state in-between alive and death, may occur. As many food applications of pulsed electric fields (PEF) rely on the complete inactivation of spoilage and pathogenic bacteria, sublethal injury is an important issue which has to be overcome. In order to detect sublethal injury or related aspects, a variety of different methods can be applied, e.g., differential plating, leakage of intracellular components, or staining. The most accurate and fast technique is the use of flow cytometry in combination with different dyes for the determination of structural and physiological aspects, i.e., membrane integrity and metabolic activity. Considering molecular stress responses, PEF induces similar pathways than oxidation stress; however the effects are not as pronounced as for heat shocks, as the main target of the PEF response is the expression of proteins related to membrane repair. After PEF treatment, sublethally injured cells might recover, depending on intrinsic, strain-specific factors, as well as the surrounding matrix properties, especially the pH, and storage time and temperature. Thus, knowledge of sublethal injury is crucial for the design of food-related PEF applications, in order to ensure high levels of food safety.

Keywords

Pulsed electric fields (PEF) Reversible and irreversible electroporation Sublethal injury Stress induction and response Inactivation and recovery 

References

  1. Aronsson K, Borch E, Stenlöf B, Rönner U (2004) Growth of pulsed electric field exposed Escherichia coli in relation to inactivation and environmental factors. Int J Food Microbiol 93(1):1–10CrossRefGoogle Scholar
  2. Aronsson K, Ronner U, Borch E (2005) Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae in relation to membrane permeabilization and subsequent leakage of intracellular compounds due to pulsed electric field processing. Int J Food Microbiol 99(1):19–32CrossRefGoogle Scholar
  3. Arroyo C, Somolinos M, Cebrian G, Condon S, Pagan R (2010) Pulsed electric fields cause sublethal injuries in the outer membrane of Enterobacter sakazakii facilitating the antimicrobial activity of citral. Lett Appl Microbiol 51(5):525–531CrossRefGoogle Scholar
  4. Cebrián G, Raso J, Condón S, Mañas P (2012) Acquisition of pulsed electric fields resistance in Staphylococcus aureus after exposure to heat and alkaline shocks. Food Control 25(1):407–414CrossRefGoogle Scholar
  5. Cebrián G, Mañas P, Condón S (2015) Relationship between membrane permeabilization and sensitization of S. aureus to sodium chloride upon exposure to pulsed electric fields. Innovative Food Sci Emerg Technol 32:91–100CrossRefGoogle Scholar
  6. Chang DC, Chassy BM, Saunders JA, Sowers AE (2012) Guide to electroporation and electrofusion. Elsevier Science, BulgariaGoogle Scholar
  7. Chueca B, Pagán R, García-Gonzalo D (2015) Transcriptomic analysis of Escherichia coli MG1655 cells exposed to pulsed electric fields. Innovative Food Sci Emerg Technol 29:78–86CrossRefGoogle Scholar
  8. Davey HM (2011) Life, death, and in-between: meanings and methods in microbiology. Appl Environ Microbiol 77(16):5571–5576CrossRefGoogle Scholar
  9. FDA (2015) Kinetics of microbial inactivation for alternative food processing technologies – pulsed electric fields. http://www.fda.gov/Food/FoodScienceResearch/SafePracticesforFoodProcesses/ucm101662.htm. Accessed 21 Nov 2016Google Scholar
  10. Garcia D, Gomez N, Condon S, Raso J, Pagan R (2003) Pulsed electric fields cause sublethal injury in Escherichia coli. Lett Appl Microbiol 36:140–144CrossRefGoogle Scholar
  11. Garcia D, Hassani M, Manas P, Condon S, Pagan R (2004) Inactivation of Escherichia coli O157:H7 during the storage under refrigeration of apple juice treated by pulsed electric fields. J Food Saf 25:30–42CrossRefGoogle Scholar
  12. Garcia D, Gomez N, Manas P, Condon S, Raso J, Pagan R (2005a) Occurrence of sublethal injury after pulsed electric fields depending on the micro-organism, the treatment medium ph and the intensity of the treatment investigated. J Appl Microbiol 99(1):94–104CrossRefGoogle Scholar
  13. García D, Gómez N, Raso J, Pagán R (2005b) Bacterial resistance after pulsed electric fields depending on the treatment medium pH. Innovative Food Sci Emerg Technol 6(4):388–395CrossRefGoogle Scholar
  14. Garcia D, Manas P, Gomez N, Raso J, Pagan R (2006) Biosynthetic requirements for the repair of sublethal membrane damage in Escherichia coli cells after pulsed electric fields. J Appl Microbiol 100(3):428–435CrossRefGoogle Scholar
  15. Garcia D, Gomez N, Manas P, Raso J, Pagan R (2007) Pulsed electric fields cause bacterial envelopes permeabilization depending on the treatment intensity, the treatment medium pH and the microorganism investigated. Int J Food Microbiol 113(2):219–227CrossRefGoogle Scholar
  16. Grahl T, Märkl H (1996) Killing of microorganisms by pulsed electric fields. Appl Microbiol Biotechnol 45:148–157CrossRefGoogle Scholar
  17. Heinz V, Alvarez I, Angersbach A, Knorr D (2001) Preservation of liquid foods by high intensity pulsed electric fields – basic concepts for process design. Trends Food Sci Technol 12(3–4):103–111CrossRefGoogle Scholar
  18. Hulsheger H, Potel J, Niemann EG (1983) Electric field effects on bacteria and yeast cells. Radiat Environ Biophys 22(2):149–162CrossRefGoogle Scholar
  19. Jaeger H, Schulz A, Karapetkov N, Knorr D (2009) Protective effect of milk constituents and sublethal injuries limiting process effectiveness during PEF inactivation of Lb. rhamnosus. Int J Food Microbiol 134(1–2):154–161CrossRefGoogle Scholar
  20. Kinosita K, Tsong TY (1977) Formation and resealing of pores of controlled sizes in human erythrocyte membrane. Nature 268(5619):438–441CrossRefGoogle Scholar
  21. Knorr D, Angersbach A, Eshtiaghi MN, Heinz V, Lee D-U (2001) Processing concepts based on high intensity electric field pulses. Trends Food Sci Technol 12(3–4):129–135CrossRefGoogle Scholar
  22. Kotnik T, Frey W, Sack M, Haberl Meglic S, Peterka M, Miklavcic D (2015) Electroporation-based applications in biotechnology. Trends Biotechnol 33(8):480–488CrossRefGoogle Scholar
  23. Lado BH, Bomser JA, Dunne CP, Yousef AE (2004) Pulsed electric field alters molecular chaperone expression and sensitizes Listeria monocytogenes to heat. Appl Environ Microbiol 70(4):2289–2295CrossRefGoogle Scholar
  24. Leistner L (1978) Hurdle effect and energy saving. In: Downey WK (ed) Food quality and nutrition. Applied Science Publishers, London, pp 553–557Google Scholar
  25. Martín-Belloso O, Sobrino-López A (2011) Combination of pulsed electric fields with other preservation techniques. Food Bioprocess Technol 4(6):954–968CrossRefGoogle Scholar
  26. Mattar JR, Turk MF, Nonus M, Lebovka NI, El Zakhem H, Vorobiev E (2015) S. cerevisiae fermentation activity after moderate pulsed electric field pre-treatments. Bioelectrochemistry 103:92–97CrossRefGoogle Scholar
  27. Mönch SBD, Stute R (2002) Process for producing yeast extracts. Patent EP 1199353. https://google.com/patents/EP1199353A1?cl=en22
  28. Neumann E, Rosenheck K (1972) Permeability changes induced by electric impulses in vesicular membranes. J Membr Biol 10(1):279–290CrossRefGoogle Scholar
  29. Pina-Pérez MC, Rodrigo D, López AM (2009) Sub-lethal damage in Cronobacter sakazakii subsp. sakazakii cells after different pulsed electric field treatments in infant formula milk. Food Control 20(12):1145–1150CrossRefGoogle Scholar
  30. Raso J (2016) Fundamental and applied aspects of pulsed electric fields for microbial inactivation. In: Jarm T, Kramar P (eds) Proceedings of the 1st world congress on electroporation and pulsed electric fields in biology, medicine and food & environmental technologies: Portorož, Slovenia, September 6–10, 2015. Springer Singapore, Singapore, pp 11–14Google Scholar
  31. Requena JM (2012) Stress response in microbiology. Caister Academic Press, MadridGoogle Scholar
  32. Rivas A, Pina-Pérez MC, Rodriguez-Vargas S, Zuñiga M, Martinez A, Rodrigo D (2013) Sublethally damaged cells of Escherichia coli by pulsed electric fields: the chance of transformation and proteomic assays. Food Res Int 54(1):1120–1127CrossRefGoogle Scholar
  33. Rodrigo M, Martinez A, Rodrigo D (2004) Inactivation kinetics of microorganisms by pulsed electric fields. In: Barbosa-Canovas GV, Tapia MS, Pila Cano M (eds) Novel food processing technologies. CRC Press, Boca Raton, pp 69–86CrossRefGoogle Scholar
  34. Sagarzazu N, Cebrián G, Pagán R, Condón S, Mañas P (2013) Emergence of pulsed electric fields resistance in Salmonella enterica serovar Typhimurium SL1344. Int J Food Microbiol 166(2):219–225CrossRefGoogle Scholar
  35. Saulis G, Satkauskas S, Praneviciute R (2007) Determination of cell electroporation from the release of intracellular potassium ions. Anal Biochem 360(2):273–281CrossRefGoogle Scholar
  36. Schwan HP (1957) Electrical properties of tissue and cell suspensions. Adv Biol Med Phys 5:147–209CrossRefGoogle Scholar
  37. Sensoy I, Zhang QH, Sastry SK (1997) Inactivation kinetics of Salmonella Dublin by pulsed electric field. J Food Process Eng 20(5):367–381CrossRefGoogle Scholar
  38. Seratlic S, Bugarski B, Nedović V, Radulović Z, Wadsö L, Dejmek P, Galindo FG (2013a) Behavior of the surviving population of Lactobacillus plantarum 564 upon the application of pulsed electric fields. Innovative Food Sci Emerg Technol 17:93–98CrossRefGoogle Scholar
  39. Seratlic S, Bugarski B, Radulovic Z, Dejmek P, Wadsö L, Nedovic V (2013b) Electroporation enhances the metabolic activity of Lactobacillus plantarum 564. Food Technol Biotechnol 51(4):446–452Google Scholar
  40. Somolinos M, Garcia D, Manas P, Condon S, Pagan R (2008) Effect of environmental factors and cell physiological state on pulsed electric fields resistance and repair capacity of various strains of Escherichia coli. Int J Food Microbiol 124(3):260–267CrossRefGoogle Scholar
  41. Spilimbergo S, Cappelletti M, Tamburini S, Ferrentino G, Foladori P (2014) Partial permeabilisation and depolarization of Salmonella enterica Typhimurium cells after treatment with pulsed electric fields and high pressure carbon dioxide. Process Biochem 49(12):2055–2062CrossRefGoogle Scholar
  42. Tanino T, Sato S, Oshige M, Ohshima T (2012) Analysis of the stress response of yeast Saccharomyces cerevisiae toward pulsed electric field. J Electrost 70(2):212–216CrossRefGoogle Scholar
  43. Ulmer H, Heinz V, Gänzle M, Knorr D, Vogel R (2002) Effects of pulsed electric fields on inactivation and metabolic activity of Lactobacillus plantarum in model beer. J Appl Microbiol 93:326–335CrossRefGoogle Scholar
  44. Wang M-S, Zeng X-A, Sun D-W, Han Z (2015) Quantitative analysis of sublethally injured Saccharomyces cerevisiae cells induced by pulsed electric fields. LWT Food Sci Technol 60(2):672–677CrossRefGoogle Scholar
  45. Wang LH, Wang MS, Zeng XA, Liu ZW (2016) Temperature-mediated variations in cellular membrane fatty acid composition of Staphylococcus aureus in resistance to pulsed electric fields. Biochim Biophys Acta 1858(8):1791–1800CrossRefGoogle Scholar
  46. Wouters PC, Dutreux N, Smelt JPPM, Lelieveld HLM (1999) Effects of pulsed electric fields on inactivation kinetics of Listeria innocua. Appl Environ Microbiol 65(12):5364–5371Google Scholar
  47. Yun O, Zeng XA, Brennan CS, Han Z (2016) Effect of pulsed electric field on membrane lipids and oxidative injury of Salmonella typhimurium. Int J Mol Sci 17(8)Google Scholar
  48. Zhang Q, Zhuang J, von Woedtke T, Kolb JF, Zhang J, Fang J, Weltmann K-D (2014) Synergistic antibacterial effects of treatments with low temperature plasma jet and pulsed electric fields. Appl Phys Lett 105(10):104103CrossRefGoogle Scholar
  49. Zhao W, Yang R, Zhang HQ, Zhang W, Hua X, Tang Y (2011) Quantitative and real time detection of pulsed electric field induced damage on Escherichia coli cells and sublethally injured microbial cells using flow cytometry in combination with fluorescent techniques. Food Control 22(3–4):566–573CrossRefGoogle Scholar
  50. Zhao W, Yang R, Shen X, Zhang S, Chen X (2013) Lethal and sublethal injury and kinetics of Escherichia coli, Listeria monocytogenes and Staphylococcus aureus in milk by pulsed electric fields. Food Control 32(1):6–12CrossRefGoogle Scholar
  51. Zhao W, Yang R, Y-j G, Tang Y, Li C (2014a) Assessment of pulsed electric fields induced cellular damage in Saccharomyces cerevisiae: change in performance of mitochondria and cellular enzymes. LWT Food Sci Technol 58(1):55–62CrossRefGoogle Scholar
  52. Zhao W, Yang R, Gu Y, Li C (2014b) Effects of pulsed electric fields on cytomembrane lipids and intracellular nucleic acids of Saccharomyces cerevisiae. Food Control 39:204–213CrossRefGoogle Scholar
  53. Zimmermann U, Pilwat G, Riemann F (1974) Dielectric breakdown of cell membranes. Biophys J 14(11):881–899CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Felix Schottroff
    • 1
  • Anna Krottenthaler
    • 1
  • Henry Jaeger
    • 1
  1. 1.Institute of Food TechnologyUniversity of Natural Resources and Life Sciences (BOKU)ViennaAustria

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